Research
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Light-dependent maintenance of hydraulic function in mangrove
branches: do xylary chloroplasts play a role in embolism repair?
Author for correspondence:
Nele Schmitz
Tel: +32 2 629 34 14
Email: [email protected]
Received: 21 February 2012
Accepted: 22 April 2012
N. Schmitz1,2,3, J. J. G. Egerton3, C. E. Lovelock4 and M. C. Ball3
1
Laboratory for Plant Biology and Nature Management, Vrije Universiteit Brussel, 1050 Brussels, Belgium; 2Royal Museum for
Central Africa, Laboratory for Wood Biology and Xylarium, Leuvensesteenweg 13, 3080 Tervuren, Belgium; 3Plant Science
Division, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia; 4The School of
Biological Science, The University of Queensland, Brisbane, Qld 4072, Australia
Summary
New Phytologist (2012) 195: 40–46
doi: 10.1111/j.1469-8137.2012.04187.x
Key words: branch photosynthesis,
embolism repair, hydraulic conductivity,
mangrove, xylary chloroplasts.
• To clarify the role of branch photosynthesis in tree functioning, the presence and function
of chloroplasts in branch xylem tissue were studied in a diverse range of mangrove species
growing in Australia.
• The presence of xylary chloroplasts was observed via chlorophyll fluorescence of transverse
sections. Paired, attached branches were selected to study the effects of covering branches
with aluminium foil on the gas exchange characteristics of leaves and the hydraulic conductivity of branches.
• Xylary chloroplasts occurred in all species, but were differently distributed among living cell
types in the xylem. Covering stems altered the gas exchange characteristics of leaves, such
that water-use efficiency was greater in exposed leaves of covered than of uncovered
branches.
• Leaf-specific hydraulic conductivity of stems was lower in covered than in uncovered
branches, implicating stem photosynthesis in the maintenance of hydraulic function. Given
their proximity to xylem vessels, we suggest that xylary chloroplasts may play a role in
light-dependent repair of embolized xylem vessels.
Introduction
Many woody species have photosynthetic stems, at least while the
stems are relatively young. Stem photosynthesis can contribute to
the growth of trunks and development of buds in young woody
plants (Saveyn et al., 2010). Most studies, however, have emphasized a role of stem photosynthesis in refixation of respired CO2.
This would reduce carbon costs associated with maintenance of
living tissues in stems, with far-reaching implications for stem
survival when foliar photosynthesis may be limited by environmental conditions such as drought (Comstock et al., 1988;
Teskey et al., 2008; Wittmann & Pfanz, 2008; McGuire et al.,
2009).
Most attention has been given to corticular photosynthesis,
particularly as high concentrations of chloroplasts can give stems
a green colour. Less obvious, however, are the chloroplasts within
living tissues of the xylem (Wiebe et al., 1974; Wiebe, 1975).
Using chlorophyll fluorescence, Dima et al. (2006) found xylary
chloroplasts to be common in a range of woody species in a
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Mediterranean habitat. These observations invite questions about
the potential role of xylary chloroplasts in repair of embolisms
and maintenance of hydraulic function. These questions arise
because recent studies have demonstrated that hydrolysis of starch
in xylem parenchyma occurs coincident with embolism repair
(Salleo et al., 2009; Zwieniecki & Holbrook, 2009; Nardini
et al., 2011; Secchi & Zwieniecki, 2011) and that prolonged
darkness inhibits embolism repair in intact rice plants (Stiller
et al., 2005).
In the present study, we used chlorophyll fluorescence to determine the distribution of xylary chloroplasts in stems of a diverse
range of mangrove species growing naturally in wet and arid
estuarine forests in Australia. We hypothesized that xylary
chloroplasts would be more common in species with white than
with dark bark, and in species growing in more saline habitats
and under more arid climatic conditions. We also covered
branches to test two hypotheses about the functions of branch
photosynthesis in mangrove species. First, if branch photosynthesis
contributes to the carbon status of branches, then we predicted
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that covering branches would increase foliar photosynthesis,
presumably in response to an increase in the demand for
assimilates to sustain covered branch tissues. Secondly, if xylary
photosynthesis contributes to the maintenance of hydraulic
function, then we predicted that hydraulic conductivity would be
lower in covered than in uncovered branches.
Materials and Methods
Study sites and sample collection
The study was conducted in mangrove forests along the estuarine
flood plains of the Daintree River (March and July 2010) in the
wet tropics of Far North Queensland, Australia, (Lat S 1620¢,
Long E 14530¢) and Giralia Bay (August 2010) in arid Western
Australia (Lat S 2243¢, Long E 11434¢) (Lovelock et al., 2011).
At the Daintree site we studied 13 species, of which only three
were available for study at Giralia Bay (Supporting Information,
Table S1). Avicennia marina was studied at three different localities in Giralia Bay that, together with the Daintree site, can be
ordered according to relative soil water salinity (Table 1).
Chlorophyll fluorescence
Chlorophyll fluorescence was used to detect the presence of
chloroplasts in branch xylem. The trees were growing naturally in
soils with pore water salinities ranging from 1 to > 50 ppt.
Branches of c. 6 mm diameter were collected, with additional
sampling of smaller or larger branches (range: 2.8–14 mm) when
the 6 mm branch either lacked chlorophyll fluorescence in the
wood or the intensity of the fluorescence decreased from pith to
bark. Branch samples of different bark thickness (range: 0–2.3
mm, Table S1), different bark colour (white, green, brown) and
bark texture (smooth or rough and fissured) were also studied.
Transverse sections (50–100 lm thickness) were cut from freshly
Research 41
sampled branches with a field portable microtome and placed in
a drop of water on glass slides for observation with a Zeiss Axiostar Plus, modified to support a Walz Chlorophyll Fluorometer
Imaging PAM M-Series Microscopy System IV (Effeltrich,
Germany). Images were collected of the spatial distribution of
the fluorescence yield in response to a saturating pulse of light
and compared with images of the same xylem tissue, under
near-infrared light, to identify the sources of chlorophyll fluorescence emissions. To interpret the fluorescence images, additional
wood sections (20–30 lm thickness) were cut and double-stained with safranin-alcian blue to visualize the amount of
ray and axial parenchyma in the xylem tissue of each species.
Chloroplast role in branch functionality
An experiment where branches were shaded from light was performed on all three species growing at Giralia Bay and on
Rhizophora apiculata, Ceriops australis and A. marina growing at
the Daintree site (Table 1). One pair of fully exposed branches,
each c. 6 mm diameter and bearing a similar leaf area, was
selected on each of five trees per species and per site. One branch
of each pair was covered with aluminium foil up to the apical
bud, leaving the leaves uncovered. The branches were allowed to
incubate for several days before gas exchange characteristics of the
leaves were measured. Finally, branches were harvested for
measurement of hydraulic conductivity.
Gas exchange characteristics of fully exposed, mature leaves
were measured in the morning, with a Li-Cor 6400 Portable
Photosynthesis System (Li-Cor Corp, Lincoln, NE, USA).
Measurements were made under ambient conditions except that
the incident light intensity was maintained at 1000 lmol quanta
m)2 s)1. Upon completion of all gas exchange measurements, the
branches were collected and immediately transported to the
laboratory for measurement of hydraulic conductivity using an
optical technique as previously described (Choat et al., 2011). A
Table 1 Data used to calculate rates of branch photosynthesis in five mangrove species assuming that increased assimilation rates in leaves compensated
for losses in assimilation rates of branches covered with aluminium foil
Covering Covered StemS Covered XylemV Covered BarkV Branch LeafS
n period (d) (cm2)
(cm3)
(cm3)
(cm2)
AL(U) (lmol
CO2 s)1 m)2) dAL (%)
Rhizophora apiculata
Ceriops australis
Aegiceras corniculatum
Rhizophora stylosa
Avicennia marina
66 ppt
55 ppt
42 ppt
17 ppt
5
5
4
4
5
6
4
4
42.6
47.2
67.7
112.4
±
±
±
±
8.4
6.7
4.4
22.0
2.8
3.3
4.6
7.8
±
±
±
±
0.9
0.8
0.6
2.5
4.3
4.2
5.1
12.6
±
±
±
±
1.0
0.4
0.6
2.8
425.7
12.4
93.5
168.3
±
±
±
±
80.7
0.7
16.1
61.4
12.9
4.8
4.9
4.8
±
±
±
±
0.9
0.2
1.1
1.4
9.2 ± 4.2 11.1 ± 5.1
)9.5 ± 9.6 )0.1 ± 0.1
36.2 ± 35.4 0.7 ± 0.9
37.0 ± 52.7 )1.9 ± 2.1
5
5
6
5
6
6
4
3
50.4
74.3
102.7
187.4
±
±
±
±
4.7
17.0
16.6
33.4
4.5
8.4
13.0
37.9
±
±
±
±
0.7
3.2
3.7
9.2
2.9
4.2
6.2
10.5
±
±
±
±
0.3
1.0
1.2
2.5
139.6
163.7
297.2
1652.4
±
±
±
±
20.2
7.0
17.0
7.2
49.9
8.2
396.1 16.4
±
±
±
±
0.2
0.5
0.9
0.6
10.9 ± 4.5
2.4 ± 1.2
)11.5 ± 5.5 )2.6 ± 1.2
5.4 ± 24.7 )0.8 ± 4.3
4.3 ± 3.7
4.8 ± 6.0
Average of 5 species
5 5
Species
85.6 ± 14.1
10.3 ± 2.7
6.2 ± 1.2
369.1 ± 80.3
8.3 ± 0.7
10.3 ± 17.5
AB (lmol
CO2 s)1 m)2)
1.7 ± 2.6
StemS, total stem surface area covered with aluminium foil; XylemV, the associated xylem volume; BarkV, bark volume; Branch LeafS, total leaf area of
covered branches.
AL, leaf assimilation rate of the associated leaves of the covered (C) and uncovered branches (U); dAL, the change in leaf assimilation rate after branch
covering; and AB, the assimilation rate of the branch, where AB = [(AL(C) ) AL(U)) · Branch LeafS] · Covered StemS)1.
Data for Avicennia marina were collected at four sites differing in soil water salinity (ppt). Values are means ± 1 SE. Overall means were calculated as the
mean of the mean values for each of the five species and sites (for A. marina).
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pressure head of 40–70 cm, generating a pressure gradient of 4–7
kPa, was imposed on branches of 8–16 cm length. Measurements
were made with a perfusion solution of 1% filtered sea water
(Stuart et al., 2007) to mimic the ionic composition of xylem sap
in most mangrove species (Scholander et al., 1966; Ball, 1988).
The flow rate was averaged over a period of 5 min with calculations based on images collected every 30 s to track the movement
of the meniscus of a coloured solution in a pipette connected to
the branch outlet. Leaf-specific hydraulic conductivity was then
calculated as the flow rate per pressure gradient, standardized for
branch length and total leaf area of the branch (KL). Images were
taken of cross-sections of the branches to measure areas occupied
by bark, xylem (excluding the pith) and total stem area in ImageJ
1.43u (http://rsb.info.nih.gov/ij/) to calculate the respective
volumes that were shaded (Table 1).
Statistics
To test if the changes in gas exchange characteristics were significantly different between covered and uncovered branches a paired
t-test was performed. The potential interacting effect of species
and site was tested via a one-way ANOVA. The differences in KL
between branches within a branch pair were tested using a paired
t-test. In cases where data were not normally distributed a log
transformation was performed. The match between KL values of
covered and uncovered branches was tested, after log transformation, by a simple linear regression. The effect of species and sites,
across species (arid vs wet) and within A. marina (sites of different soil water salinity, see Table 1), was tested via an analysis of
covariance (ANCOVA).
Results
Distribution of chloroplasts in branch xylem
Chlorophyll fluorescence was detected in the xylem of all studied
tree species, although to a lesser extent in Bruguiera sexangula and
Rhizophora stylosa than in the other species. The maximum diameter of branches in which fluorescence was observed in the
wood varied from 6 to 13 mm across the studied species (Table
S1). Within a branch, chlorophyll fluorescence typically
decreased with depth from bark to pith, except in Ceriops spp.
where branches with a relatively thick bark only showed chlorophyll fluorescence near the pith. Between branches of increasing
bark thickness, the distribution of chlorophyll fluorescence in the
xylem generally decreased, from being present along the entire
branch radius to only near the bark. However, the presence of
chlorophyll fluorescence and that of bark thickness were not
strictly related. Also branch diameter and colour of the bark were
unrelated to the distribution of chlorophyll fluorescence. Even
within a species, branches that showed chlorophyll fluorescence
could be thicker and ⁄ or have a thicker bark than branches without fluorescence.
No relationship was found between the spatial distribution of
axial parenchyma and chlorophyll fluorescence (Fig. 1). Eight
species showed chlorophyll fluorescence only in the rays (Table
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S1), amongst which Sonneratia caseolaris, Xylocarpus granatum
and Heritiera littoralis had moderate to abundant axial parenchyma (Fig. 1c–e). The two studied Ceriops species and
A. marina showed chlorophyll fluorescence in rays and
vessel-associated parenchyma cells (Table S1, Figs 1b, 3c,d). In
R. apiculata, chlorophyll fluorescence occurred only in the
vessel-associated cells (Fig. 1a).
Effects of covering branches on shoot functions
There were no significant effects of covering branches on either
the assimilation rate or stomatal conductance. Nevertheless, covering branches significantly increased leaf-level water-use efficiency (paired t = )2.18, n = 39, P = 0.03), as measured by the
ratio of assimilation rate to stomatal conductance, and decreased
the intercellular CO2 concentrations (paired t = 2.10, n = 39,
P = 0.04) (Fig. 2a). The results were variable (Fig. S1) but there
were no significant effects of either species (F = 1.88, df = 4,
P = 0.14) or sites (F = 0.66, df = 3, P = 0.58). Although not
significant, the mean assimilation rates of leaves attached to
covered branches were 10.3% greater than those of uncovered
branches on the same trees (Table 1). This higher mean value
was driven by the occurrence of higher assimilation rates in leaves
of covered branches in 56% of branch pairs. Nevertheless, maintenance of a constant or greater assimilation rate with decrease
in intercellular CO2 concentration and increase in water-use
efficiency requires up-regulation of photosynthesis in response to
the covering of branches.
Covering branches also affected leaf -specific hydraulic conductivity of the stems, KL. Despite variability (Fig. S1), all species
responded similarly (Fig. 2b, F = 0.38, df = 4, P = 0.82) with
no significant effect of climatic conditions (Fig. 2b, F = 0.057, df
= 1, P = 0.81) or of local variations in soil water salinity for the
different sites of A. marina (Fig. 2b, F = 2.79, df = 3, P = 0.06).
The linear relationship between KL of covered and uncovered
branches shows that the branches were well matched within each
tree, despite the large range of KL values between individual trees
of the same and different species (Fig. 2b, r = 0.76, F = 38.04,
P < 0.0001). Averaged over the whole study, KL was significantly
lower in covered than in uncovered branches (Fig. 2c, paired
t = 3.34, n = 29, P = 0.002). This equated to a median loss in
hydraulic conductivity of c. 50% in covered branches (and a
mean loss of 26% based on the log10-transformed data, Fig. 2c).
Discussion
The results of the present study show that xylary chloroplasts are
a common feature of mangrove wood (Table S1, Fig. 1). This is
consistent with the occurrence of chloroplasts in the wood of
species from other biomes (Wiebe et al., 1974; Wiebe, 1975;
Wittmann et al., 2001; Pilarski & Tokarz, 2006), including 20
species with diverse phenological behaviour in Greece (Dima
et al., 2006).
The spatial distribution of chloroplasts within branches is
suggestive of interspecific differences in axial and radial light
transmission and guidance through branch tissues. In most
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(a)
(b)
(c)
(d)
(e)
Fig. 1 Chlorophyll fluorescence (column 1) demonstrates the presence of xylary chloroplasts in vessel-associated parenchyma cells and ray cells (column 2)
in transverse sections of branches of five mangrove species. There is no link between the species-specific distribution of vessel-associated parenchyma cells
(column 3) and chlorophyll fluorescence. Species are ordered in terms of relative amounts of vessel-associated parenchyma cells. Transverse wood sections
in column 3 are of the same species but from different branches of larger diameter, except for (c) where the branch was smaller than the one used for
column 2. Sections were stained with safranin-alcian blue, distinguishing parenchyma (blue) from fibres and vessels (pink). (a) Rhizophora apiculata; (b)
Ceriops decandra; (c) Sonneratia caseolaris; (d) Xylocarpus granatum; (e) Heritiera littoralis. Bars, 100 lm.
species, the rays were the main light guides (Fig. 1b–e,
Table S1), transmitting the light from the bark inwards.
Additionally, in a few species, with Ceriops spp. as the clearest
example, the spatial patterns of chlorophyll fluorescence revealed
the presence of abundant chloroplasts in the pith. As all studied
branches were relatively close to the apex, this is suggestive of
axial light transmission (Sun et al., 2003) through the pith.
Similarly, Vancleve et al. (1993) found photosynthetically active
chloroplasts in the stem pith of poplar, a woody species with
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white bark. Our findings indicate that the presence of xylary
chloroplasts along the branch radius depended on the lightguiding properties of the bark, partly related to the bark thickness
but independent of its colour. Nevertheless, the maximum diameter and stem depth at which xylary chloroplasts occurred could
not be linked to any single factor, such as bark thickness or colour, but presumably depended on a complex combination of
transmittance and light-guiding properties of wood (Sun et al.,
2003) and bark tissues (Trockenbrodt, 1991, 1994).
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(a)
(b)
(c)
Fig. 2 Effects of covering branches with aluminium foil on the gas
exchange and hydraulic characteristics of associated leaves and branches,
respectively, in five mangrove species. (a) Percentage change in covered
vs uncovered branches (means ± 1 SE) in the ratio of CO2 assimilation
rate to stomatal conductance (A ⁄ g) and the intercellular CO2
concentration (Ci). Species are ordered according to increasing stem area
covered (Table 1). (b) Log-transformed leaf-specific hydraulic conductivity
(KL), matched well between uncovered (U) and covered (C) branch pairs in
an arid (open and grey symbols) and wet (closed symbols) coastal system.
Avicennia marina occupied different local sites within the arid system
categorized from low to high soil water salinity (see Table 1).
(c) Averaging sites and species, the mean (± 1 SE) of the log-transformed
leaf-specific hydraulic conductivity (KL) for covered branches was
significantly lower than for uncovered branches. Ac, Aegiceras
corniculatum; Am, Avicennia marina; Ca, Ceriops australis; Ra,
Rhizophora apiculata; Rs, Rhizophora stylosa.
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Photosynthesis by chloroplasts within bark and stem tissues
can contribute to the carbon and water balances of these tissues
(Pfanz et al., 2002; Aschan & Pfanz, 2003). Stem photosynthesis
is believed mainly to involve refixation of respired CO2, thereby
reducing carbon losses from the stems. We expected leaf photosynthetic rates to increase if the covering of stems increased their
demands for carbon assimilates needed to maintain cellular functions. Contrary to our predictions, covering branches did not
significantly increase assimilation rates in associated leaves,
although assimilation rates in leaves of covered branches were on
average 10.3% higher than those of control, uncovered branches
(Table 1). Three explanations could be given for the variable
response of the branches (Fig. S1), both within and between
species: the short experimental period, relative to the resilience of
the photosynthetic apparatus to darkness (Parolin, 2008); the
need for the trees to compensate the loss in photosynthates,
which is related to the local environmental conditions; and the
ability to up-regulate photosynthesis in uncovered parts of the
branch instead of in leaves.
How large is the contribution of branch photosynthesis to the
carbon balance of shoots? An increase of 10.3% in assimilation
rates of leaves attached to covered branches might seem small.
However, if we assume that the higher leaf assimilation rates fully
compensated for losses in photosynthetic activity of covered
branches, and that all leaves within a branch behave similarly,
then the average increase in leaf assimilation rates corresponds to
an average stem assimilation rate of 1.7 lmol CO2 m)2 s)1
(Table 1). This rate is consistent with a recent estimate based on
different methods of 1.5 lmol CO2 m)2 s)1 for corticular photosynthesis in a eucalypt species (Cernusak & Hutley, 2011).
Photosynthetic assimilation rates in stems thus could be c. 20%
of the average rates in leaves (Table 1; 1.7 lmol CO2 m)2
s)1 ⁄ 8.3 lmol CO2 m)2 s)1 · 100) and could contribute c. 5%
of the total assimilation rate of an average branch (Table 1; 1.7
lmol CO2 m)2 s)1 · 85.6 10)4 m2 ⁄ 8.3 lmol CO2 m)2 s)1 ·
369.1 10)4 m2). However, it would be incorrect to conclude
from these calculations that changes in assimilation rates were
sufficient to compensate for losses in stem photosynthesis, as
more data would be needed to determine the carbon balance.
Nevertheless, the potential contribution of bark and wood photosynthesis to the carbon balance of a tree underscores the suggestion that the unexpected daytime decrease in CO2 efflux,
observed in beech and oak, is the result of C refixation (Saveyn
et al., 2008). This could be extremely important under natural
conditions as bark and wood photosynthesis could support the
maintenance costs of the stem during times when environmental
conditions constrain photosynthetic activity in leaves (Vick &
Young, 2009; Cernusak & Hutley, 2011), such as during
drought.
As carbon cannot be gained without the expenditure of water,
recapture of respired CO2 by stem photosynthesis effectively
reduces shoot water losses, thereby enhancing water-use efficiency
(Eyles et al., 2009). Such savings in both carbon and water may
contribute to survival in environments where water availability
may be limited by seasonal drought or high soil salinity. Indeed,
leaf-level water-use efficiency significantly increased within 1 wk
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(a)
(b)
(c)
(d)
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Fig. 3 The relative amount of vessel-associated parenchyma cells in Avicennia marina branch wood is higher in a site of relatively high salinity (a) than in
one of low (b) soil water salinity. Transverse wood sections are stained with safranin-alcian blue, distinguishing parenchyma (blue) from fibres and vessels
(pink). Chlorophyll fluorescence (c) indicates the presence of chloroplasts in both rays and vessel-associated parenchyma cells (d). Bars, 100 lm.
of covering branches (Fig. 2a), underscoring the importance of
stem photosynthesis for both carbon and water balances.
Finally, the loss in KL following branch covering provides evidence that stem photosynthesis contributes to maintenance of
hydraulic function. Like other plant species, mangroves typically
operate near their cavitation threshold, which varies with the prevailing salinity of their habitat (Sperry et al., 1988; Melcher
et al., 2001). Hence the capacity to repair embolized vessels is
essential for maintenance of hydraulic function regardless of
whether the plants grow in high- or low-salinity environments.
Indeed, diurnal variation in hydraulic conductivity of mangrove
stems has been correlated with variation in the extent to which
xylem vessels were embolized in both coastal and estuarine environments (Melcher et al., 2001). Refilling of embolized vessels
occurs coincident with loss of starch from the xylem parenchyma,
consistent with hypothetical use of sugars to create an osmotic
driving force to refill embolized vessels (Salleo, 2006; Salleo
et al., 2009; Zwieniecki & Holbrook, 2009). The effects of
corticular and xylary photosynthesis are confounded in the
present study. Nevertheless, the distribution of xylary chloroplasts in rays and in axial parenchyma cells associated with vessels,
which are more abundant in trees from the arid than the wet site
(Fig. 3), is consistent with a role for xylary chloroplasts in the
local provision of energy and photosynthates for embolism
repair, and merits further study. Thus, while their contribution
to stem photosynthesis is overshadowed by corticular activity,
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xylary chloroplasts may play a critical role in the carbon and
water balances of plants.
Acknowledgements
We thank Catherine Bone and Nigel Brothers for their invaluable
assistance with field work and Brendan Choat for assistance with
setting up the system to measure hydraulic conductivity. N.S.
was funded by a postdoctoral fellowship and a mobility grant
from The Research Foundation – Flanders (FWO). This research
was supported by Australian Research Council Discovery Project
Grant DP1096749 to M.C.B. and C.E.L.
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Supporting Information
Additional supporting information may be found in the online
version of this article.
Fig. S1 Frequency of branch pairs of five mangrove species
affected in gas exchange and stem hydraulic properties after covering one branch of the pair with aluminium foil.
Table S1 Description of chlorophyll fluorescence, indicating the
presence of xylary chloroplasts, in branch xylem of 13 mangrove
tree species of nine genera and seven families studied in a wet and
arid mangrove forest
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