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Impact of elevated atmospheric humidity on anatomical and hydraulic traits

of xylem in hybrid aspen

Article  in  Functional Plant Biology · June 2015

DOI: 10.1071/FP14224

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CSIRO PUBLISHING
Functional Plant Biology
http://dx.doi.org/10.1071/FP14224

Impact of elevated atmospheric humidity on anatomical

and hydraulic traits of xylem in hybrid aspen

nska A,B,D, Meeli Alber A, Arvo Tullus A, Märt Rahi C and Arne Sellin A
Anna Katarzyna Jasi

A
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia.
B
Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland.
C
Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 5,
51014 Tartu, Estonia.
D
Corresponding author. Email: jasiak9@wp.pl

Abstract. This study was performed on hybrid aspen saplings growing at the Free Air Humidity Manipulation site in
Estonia. We investigated changes in wood anatomy and hydraulic conductivity in response to increased air humidity.
Two hydraulic traits (specific conductivity and leaf-specific conductivity) and four anatomical traits of stem wood –
relative vessel area (VA), vessel density (VD), pit area and pit aperture area – were influenced by the humidity manipulation.
Stem hydraulic traits decreased in the apical direction, whereas branch hydraulic characteristics tended to be greatest in
mid-canopy, associated with branch size. A reduction in VD due to increasing humidity was accompanied by a decrease in
vessel lumen diameter, hydraulically weighted mean diameter (Dh), xylem vulnerability index and theoretical hydraulic
conductivity. VA and Dh combined accounted for 87.4% of the total variation in kt of branches and 85.5% of that in stems
across the treatments. Characters of branch vessels were more stable, and only the vessel-grouping index (the ratio of the
total number of vessels to the total number of vessel groupings) was dependent on the interactive effect of the treatment
and canopy position. Our results indicate that the increasing atmospheric humidity predicted for high latitudes will result
in moderate changes in the structure and functioning of the hybrid aspen xylem.

Additional keywords: atmospheric humidity, bordered pits, canopy position, hydraulic conductivity, vessel diameter,
wood anatomy.
Received 11 August 2014, accepted 17 February 2015, published online 20 March 2015

Introduction
The impacts of global warming have been studied in various
plant communities (Delucia et al. 2000; Dessler and Sherwood
2009). The consequences of climate change are not only a
matter of increasing air temperature or CO2, but also depend
on the positive feedback of atmospheric water vapour
amplifying this effect (Held and Soden 2000). Future increases
in temperature will be accompanied by a rise in absolute
atmospheric humidity on a global scale. The climate change
projections predict that annual precipitation will also increase
in northern Europe, and in particular, in the Baltic region by
5–30% (Kont et al. 2003). More frequent rain events inevitably
cause increases in relative air humidity on local or regional scales,
which may have a substantial influence on the functioning
and structure of living organisms. The general response of
trees to warmer air temperatures and increasing air humidity is
difficult to predict. Effects will be realised through modifications
in physiology, canopy architecture, anatomical structure and
morphology (Saxe et al. 2001).
Until now, researchers have paid little attention to the impact
of atmospheric humidity, although it has been widely
acknowledged that precipitation is the most relevant factor
affecting plant structure on a global scale (Moles et al. 2009).
Journal compilation
CSIRO 2015
Much more attention has been paid to the potential for more
frequent droughts. The relationship between water deficit and the
anatomical traits of xylem is fairly well explored (Plavcova and
Hacke 2012). Drought affects many structural traits of xylem
tissue, such as vessel size and shape, number of vessels
(Castro-Diez et al. 1998), growth ring width and wood density
(Koprowski and Duncker 2012). Drought results in a reduction
in vessel lumen diameter/area and number of vessels (Galle
et al. 2010; Fonti et al. 2013), but an increase in vein density
in leaves (Bresta et al. 2011): these effects are evident in diverse
plant species (Lovisolo and Schubert 1998).
Plavcova and Hacke (2012) suggested that changes in xylem
structure are difficult to predict and depend simultaneously on
many factors. Olson et al. (2014) proposed that regardless of
environment, plant size is the main driver of global variation in
mean vessel diameter. However, the altitudinal, latitudinal and
longitudinal diversification in wood anatomy is well documented,
but the causal relationships with environmental variables
remain largely unknown (Noshiro and Baas 2000). Swenson
and Enquist (2007) suggested that wood density depends on
both elevation and latitude. Noshiro and Baas (2000), per contra,
revealed that neither latitudinal nor altitudinal trends were
detected in Cornus wood traits, including vessel length,
www.publish.csiro.au/journals/fpb
B Functional Plant Biology
frequency and diameter or vessel-grouping index (the total
number of vessels divided by the total number of vessel
groups, as in work by Carlquist 2001).
The adaptive variation in hydraulic characteristics – xylem
specific conductivity or stem hydraulic conductance – has been
widely studied with respect to anatomical traits (Fan et al. 2012;
Zhang et al. 2013). Trade-offs exist between xylem structure
and function – trees must maintain sufficient hydraulic
efficiency without simultaneously being at risk of a massive
embolism (Hacke and Sperry 2001; Vinya et al. 2013). An
increase in the vessel number can compensate for the loss of
hydraulic conductivity resulting from a reduction in vessel size
(Lovisolo and Schubert 1998). It is also generally accepted that
xylem conduit size and the related hydraulic conductance
increase from twigs to primary branches and basipetally down
along the stems (Tyree and Zimmermann 2002). In addition, the
properties of intervessel pits are very important in controlling
hydraulic efficiency of xylem (Domec et al. 2006). However,
there is no published information on how air humidity and
canopy position influence differentiation of the bordered pits.
Knowledge of the long-term effect of increasing atmospheric
humidity on plant structure and functioning is still scant
(Okamoto et al. 2009; Tullus et al. 2012; Niglas et al. 2014;
Sellin et al. 2014). A Free Air Humidity Manipulation
experiment (FAHM, Estonia) conducted on two deciduous
woody species revealed an inhibitory effect of elevated
humidity on both photosynthetic capacity and growth rate in a
moderately humid temperate climate (Tullus et al. 2012; Sellin
et al. 2013). The humidification treatment caused a significant
reduction in both stem-wood (P = 0.001) and branch-wood
(P = 0.018) density in saplings of Betula pendula Roth (Sellin
et al. 2013), reflecting a change in xylem anatomical structure.
It is important to note that changes in xylem density have
significant consequences on both wood mechanical properties
(Jacobsen et al. 2007) and several functional traits associated
with its water transport capacity (Pratt et al. 2007).
This study was undertaken with the expectation that xylem
responses to artificially elevated air humidity may also occur
in hybrid aspen (Populus tremula L.
Populus tremuloides
Michx.). We hypothesise that increased air humidity induces
changes in xylem anatomical structure, primarily a decrease in
vessel density and/or vessel diameter – the main variables
determining xylem water permeability – due to decreased
water flux through the plants. These changes may also be
linked to a reduction in the vessel-grouping index, as well as
the size and number of bordered pits, as a result of the diminished
demand for effective conducting tissue under lower atmospheric
evaporative demand. The expected changes will have an
inevitable effect on plant hydraulic properties, including stem
and branch hydraulic conductance, xylem specific conductivity
and vulnerability to cavitation. This study broadens our
understanding of the ability of trees to acclimate to the
increasing atmospheric humidity predicted for northern Europe.
Materials and methods
Study area and experimental setup
The studies were conducted out using 6-year-old hybrid
aspens (Populus tremula L.
Populus tremuloides Michx.) in
A. K. Jasi

nska et al.
an experimental forest plantation at the FAHM site, situated
at Rõka village (58140 N, 27170 E, 40–48 m above sea level)
in eastern Estonia. The study site, established on an abandoned
agricultural field in 2006–07, is a fenced area of 2.7 ha
containing circular experimental plots 14 m in diameter
(10 000 trees ha–1) in which atmospheric humidity is artificially
manipulated. The computer-operated FAHM system, based
on an approach integrating two different technologies: a
misting technique to atomise/vaporise water and a FACE-like
technology to mix humidified air inside the plots, enables
relative humidity of the air (RH) to increase by up to 18%
over the ambient level during humidification application (H
treatment), depending on the wind speed inside the
experimental stand. In control plots (C treatment) the trees are
grown under ambient conditions. A detailed description of the
FAHM site and technical setup is presented in work by Kupper
et al. (2011). The treatment was started in June of 2008;
hydraulic measurements and wood sampling were performed
on nine H and nine C trees in July–August of 2011.
Hydraulic measurements
Three branches and three stem segments from each sample tree
were sampled for hydraulic properties. The sample branches
were cut from three heights in the canopy: on average at 88 cm
(mean length 97 cm, lower position), 234 cm (mean length
121 cm, medium position) and 353 cm (mean length 95 cm,
upper position) above the ground (Table 1). The cut ends were
recut under water and the branches immediately hydraulically
measured under the photosynthetic photon flux density, or
PPFD of ~150 mmol m–2 s–1 (Master SON-T PIA Agro lamps,
400 W; Philips, Eindhoven, The Netherlands). Hydraulic
conductance of bare branches (KB) was determined after leaf
removal by the water perfusion method using a high-pressure
flow meter (HPFM-Gen3; Dynamax, USA) applied in a quasi-
steady-state mode.
After achieving stable readings with the HPFM for the
leafless branch, the distal part of the branch was cut off. The
remaining 15–20 cm basal segment of the branch left connected
Table 1. Morphological data (mean þ s.e.) of sample branches
For all characteristics the treatment (C, control; H, humidification) effect
was insignificant and the effect of canopy position was statistically
significant (P < 0.05). Different letters denote significant differences
among the means
Characteristic Treatment Canopy position
Lower Medium Upper
Length (cm) C 100 ± 12.5a 123 ± 17.2a 100 ± 4.4a
H 94 ± 5.5a 119 ± 8.1a 91 ± 7.5a
Basal diameter C 6.12 ± 0.71a 7.92 ± 1.02a 7.06 ± 0.42a
measured H 5.94 ± 0.46a 8.02 ± 0.50a 6.71 ± 0.31a
under bark (mm)
Leaf area (cm2) C 1540 ± 597a 2775 ± 665b 1080 ± 106a
H 975 ± 118a 2535 ± 351b 899 ± 83a
Huber value C 2.44 ± 0.31a 1.95 ± 0.13a 3.75 ± 0.24b
(
104 m2 m–2) H 3.31 ± 0.69ab 2.01 ± 0.11a 4.08 ± 0.21b
Air humidity affects hybrid aspen xylem traits Functional Plant Biology C

(a) (b)

(c) (d )

50 um

(e) (f )

10 µm EHT = 15.00 kV Signal A = SE1 Date :7 Jan 2014 2 µm EHT = 15.00 kV Signal A = SE1 Date :7 Jan 2014
WD = 8.0 mm Photo No. = 205 Time :12:38:37 WD = 8.5 mm Photo No. = 200 Time :12:13:14

Fig. 1. Transection of wood of Populus tremula
Populus tremuloides: (a) branch, control plot; (b) branch, humidification; (c) stem, control plot;
(d) stem, humidification; (e) scanning electron microscope photograph of the inner (lumen) surface of vessel; control plot; ( f ) scanning electron
microscope photograph of the pit field with pits (a) and pit apertures (b); control plot.
D Functional Plant Biology A. K. Jasi

nska et al.

to the pressure coupling was perfused again to calculate Table 2. Results of ANOVA for effects of the humidification treatment,
the specific hydraulic conductivity of branch wood (kB), as experimental plots and canopy position on hydraulic traits
follows: ns, not significant at P < 0.05
K seg  l
kB ¼ ð1Þ Dependent Effect Statistical Partial h2
AX variable significance
where Kseg is the hydraulic conductance of the branch segment, Branch hydraulic Treatment ns –
l is the length of the segment, and AX is the cross-sectional area conductance, KB Plot (nested in Treatment) P = 0.027 0.208
of the xylem. For technical reasons, kB in the upper-canopy Canopy position P < 0.001 0.501
position could not be measured. After the hydraulic
measurements, all leaves were collected and the total area of Specific Treatment ns –
the leaf blades was measured with a LI-3100C optical area meter conductivity of Plot (nested in Treatment) ns –
(Li-Cor Biosciences, Lincoln, NE, USA). Next, the stem branch wood, kB Canopy position P < 0.001 0.394
segments (15–20 cm long) were sampled for specific hydraulic
Leaf-specific Treatment ns –
conductivity (kS) in the manner described for the branch basal conductivity of Plot (nested in Treatment) ns –
segments. The stem specimens were also cut from three branch wood, Canopy position P = 0.001 0.301
positions: on average from heights of 296, 159 and 20 cm LSCB
above the ground. The hydraulic characteristics obtained with
Branch wood Treatment ns –
the HPFM-Gen3 were corrected for the dynamic viscosity of
density, rB Plot (nested in Treatment) P = 0.013 0.238
water at 25C; the KB data were normalised to the foliage Canopy position P < 0.001 0.598
area supported by particular branches. The leaf specific
conductivity (LSC) is expressed per unit leaf area supported Specific Treatment P = 0.003 0.173
by a particular branch or stem segment (instead of unit xylem conductivity of Plot (nested in Treatment) P = 0.003 0.285
cross-sectional area). Altogether, 54 branches and stem stem-wood, kS Canopy position P < 0.001 0.300
segments (2 treatments
3 sample plots
3 trees
3 canopy
positions/heights) were assessed for hydraulic properties. After Leaf-specific Treatment P = 0.021 0.111
hydraulic measurements, the wood samples were dried to conductivity of Plot (nested in Treatment) P = 0.002 0.295
constant weight at 80C. Wood density (r) was calculated as stem wood, Canopy position P < 0.001 0.313
LSCS
specimen dry mass divided by fresh volume calculated from
the dimensions of the specimen, approximated to a frustum of Stem wood Treatment ns –
an elliptical cone. Huber values (HV) were calculated as the density, rS Plot (nested in Treatment) P < 0.001 0.413
cross-sectional area of stems or branches divided by the foliage Canopy position P < 0.001 0.321

50 2.5

40 2.0
LSCs (×10–2 kg m–1 s–1 MPa–1)
ks (kg m–1 s–1 MPa–1)

30 1.5

20 1.0

10 0.5

0 0
Lower Medium Upper
Stem segment

Fig. 2. Variation in specific (kS) and leaf-specific conductivity of stem wood (LSCS) with treatment
(C, control; H), humidification) and stem segment position. Error bars indicate  s.e. of the means;
different letters denote statistically significant (P < 0.05) differences.
Air humidity affects hybrid aspen xylem traits Functional Plant Biology E

area supported by the corresponding stem or branch sections. X

n pffiffiffiffiffiffiffiffiffiffiffi
Mean radial growth rate of branches (DDB) and stems (DDS) ai  bi
was calculated by dividing sample radius by the number of i¼1
ð3Þ
Dv ¼ ;
growth rings. n
where ai and bi are minor and major perpendicular lumen
Anatomical measurements diameters of the ith vessel, and n is the number of measured
vessels. Relative area of vessels (VA) was calculated as (total
Light microscopy vessel lumen area
100)/image area occupied by the xylem (%),
The dried wood samples were softened in 1 : 1 (v : v) 70% measured using ImageJ software. The vulnerability index (Ivul)
ethanol and glycerine solution, and slices of 15–20 mm thickness was calculated to assess xylem susceptibility to embolism
were cut with a SM2000R sliding microtome (Leica (Arbellay et al. 2012):
Microsystems, Nussloch, Germany). The slices were stained
with safranin, rinsed with water and mounted in Canada I vul ¼ Dv =VD: ð4Þ
balsam. Digital images at 100
magnification covering four
growth rings (formed in 2008–11, depending on sample Greater values of Ivul indicate greater xylem functional
origin: upper branch – one ring, lower stem samples – four vulnerability to water stress. On the basis of the vessel
rings) were taken of each wood sample (Fig. 1a–d) using an contribution to hydraulic conductance, we calculated a
Eclipse 50 light microscope equipped with a DS-Fi1 digital hydraulically weighted mean diameter (Dh) for each sample
camera (Nikon Corp., Tokyo, Japan). The vessel density (VD; (Sellin et al. 2008):
number of vessels per mm2) and grouping index (VG; Carlquist
2001) were measured with ImageJ (NIH, USA) software X
n pffiffiffiffiffiffiffiffiffiffiffi
ð ai  bi Þ5
as follows:
i¼1
Nt Dh ¼ Xn pffiffiffiffiffiffiffiffiffiffiffi : ð5Þ
VG ¼ ; ð2Þ
Ns þ Ng ð ai  bi Þ4
i¼1
where Nt is the total number of vessels, Ns is the number of
solitary vessels, and Ng is the number of vessel groups. A theoretical specific conductivity of the xylem (kt,
The minor and major vessel inner diameters (mm) and kg m–1 s–1 MPa–1; sensu Tyree and Ewers 1991) was used to
cross-sectional area of vessel lumina (mm2) were measured characterise the xylem conducting efficiency expressed
with WinCELL software (Regent Instruments, Sainte-Foy, per sapwood transverse area. In fact, kt reflects lumen
Canada). Mean vessel diameter (Dv) was calculated as a conductance, omitting the resistance between vessels. It was
geometric mean: calculated according to work by Lewis and Boose (1995):

15 3
KB (×10–3 kg m–2 s–1 MPa–1)
kB (kg m–1 s–1 MPa–1)

10 2

5 1

0 0
Lower Medium Upper

Canopy position

Fig. 3. Variation in specific conductivity of branch wood (kB) and branch hydraulic conductance
(KB) with treatment (C, control; H, humidification) and canopy position.
F Functional Plant Biology A. K. Jasi

nska et al.

(a) (b)
R 2 = 0.465, P < 0.001
Specific conductivity, k B

Specific conductivity, k B
20 20
Control Humidification
(kg m–1 s–1 MPa–1)

(kg m–1 s–1 MPa–1)

15 15

10 10

5 R 2 = 0.446, P < 0.001 5

Control Humidification
0 0
0.40 0.44 0.48 0.52 0.56 0.5 1.0 1.5 2.0 2.5 3.0
Branchwood density, ρB (g cm–3) Radial growth rate, ΔDB (mm yr–1)

Fig. 4. Density of branch wood (a, rB) and branch radial growth rate (b, DDB) versus hydraulic conductivity
of branch wood (kB).

prw X n
a3i  b3i Table 3. Comparison of xylem characteristics (mean þ s.e.) d.f. = 52
kt ¼ ; ð6Þ Different letters denote statistically significant (P < 0.05) differences
64hAX i ¼ 1 a2i þ b2i
between the treatments (xy) and the sample position (ab)
where rw is the density of water (kg m–3), AX is the sampled
cross-sectional area of xylem (m2), and h is the dynamic Characteristic Origin Control Humidification
viscosity of water (MPa s). All measurements were conducted Vessel lumen branch 26.4 ± 0.6a 26.4 ± 0.6a
on separate growth rings. Weighted means for particular sample diameter, Dv stem 37.3 ± 0.6b 36.7 ± 0.6b
were calculated as follows:
Vessel lumen branch 630 ± 30.3a 632 ± 30.3a
A 1 x1 þ A 2 x2 þ . . . þ A n xn area, Av stem 1280 ± 42.8b 1229 ± 42.8b
x¼ ð7Þ
A1 þ A2 þ . . . þ An Vessel-grouping branch 1.67 ± 0.02a 1.70 ± 0.02a
index, VG stem 1.65 ± 0.02a 1.69 ± 0.02a
where xi denotes the mean value for ith growth ring, and Ai the
respective growth ring area. Relative vessel branch 13.2 ± 0.5a 12.5 ± 0.5a
area, VA stem 16.7 ± 0.4bx 15.0 ± 0.4by
Scanning electron microscopy Vessel density, branch 273 ± 12.4a 273 ± 12.4a
Oven-dried stem-wood specimens were split in a radial VD stem 203 ± 6.0bx 184 ± 6.1by
direction with a microtome knife and were fixed on a stub Xylem branch 133 ± 14.1a 134 ± 14.1a
with double-sided carbon-based adhesive discs. The slices vulnerability stem 260 ± 9.2b 264 ± 9.2b
were coated with gold in a modified sputter-coating device index, Ivul
(VUP, Russia). All samples were examined with a Zeiss Hydraulically branch 31.0 ± 0.8a 31.0 ± 0.8a
EVO LS15 scanning electron microscope (Carl Zeiss weighted mean stem 44.7 ± 0.7b 43.76 ± 0.7b
Microscopy, Jena, Germany) in secondary electron mode at diameter, Dh
15 kV. Micrographs were taken from rings formed in 2010–11, Theoretical branch 3.26 ± 0.3a 3.18 ± 0.3a
stored at 1024
768-pixel resolution (Fig. 1e, f) and were specific stem 7.05 ± 0.4bx 5.73 ± 0.4by
analysed using ImageJ software. Pit membrane and pit conductivity, kt
aperture measurements were carried out on four to nine vessels
Wood density, r branch 0.43 ± 0.01a 0.43 ± 0.01a
per wood sample with a total number of 538 pits for C plots
stem 0.36 ± 0.01b 0.37 ± 0.01b
and 539 for H plots. Pit membrane area (Apit), pit aperture area
(Aap), pit density (number of pits per unit pitfield area, PD) and Specific hydraulic branch 9.57 ± 1.1a 9.98 ± 1.08a
pitfield fraction (percentage of the pit membrane area per unit conductivity, k stem 33.2 ± 1.8bx 40.0 ± 1.8by
pitfield area, PF) were calculated according to work by Schmitz Branch hydraulic branch 1.4 ± 0.3
103 1.1 ± 0.2
103
et al. (2007). conductance, KB

Data analysis
Statistical data analysis was conducted using Statistica, ver. 7.1
(StatSoft Inc., Tulsa, OK, USA), JMP (SAS Institute, Cary,
NC, USA) and R software (R Foundation for Statistical
Computing, Vienna, Austria). The effect of humidification on
plant hydraulic traits and radial growth rate was assessed by
applying a nested analysis of variance (ANOVA) with three
factors: ‘Treatment’, ‘Experimental plot’ (nested in the first)
and ‘Canopy position’. Thus, the Treatment effects (d.f. = 1)
were tested against the Experimental plot (d.f. = 4) and Sample
position effects (d.f. = 2); Type III sums of squares were used
Air humidity affects hybrid aspen xylem traits Functional Plant Biology G

in the calculations. In statistical analysis, mean values of Results

anatomical characteristics weighted by ring area were
used (DeBell et al. 2002). The effect of humidification on
anatomical characteristics was assessed by applying a two-
way ANOVA with fixed effects of ‘Treatment’ and ‘Canopy
position’; Type IV sums of squares were used. Effect sizes were
estimated by partial eta-squared (h2partial), defined as the ratio of
variance accounted for by an effect and that effect plus its
associated error variance:
SSeffect
h2partial ¼ ; ð8Þ
SSeffect þ SSerror
where SSeffect is the sum of squares for a given effect and SSerror
is the sum of squares for the corresponding error term. Normality
of data and homogeneity of variances were checked using
Lilliefors’ and Levene’s tests respectively. When appropriate,
logarithmic or complex transformations were applied to the
data. Post hoc mean comparisons were conducted using the
Tukey’s HSD test. Bivariate relationships between the studied
characteristics and independent variables were assessed using
simple linear or non-linear least-squares regression. Plasticity
indices (PI) of key traits were calculated according to work by
Couso and Fernández (2012):
xmax  xmin
PI ¼ ; ð9Þ
xmax
where xmax and xmin denote maximum and minimum weighted
averages of the wood samples.
Hydraulic characteristics and growth rate
All hydraulic traits – branch hydraulic conductance (KB),
specific conductivity of branch wood (kB) and stem wood (kS),
leaf-specific conductivity of branch wood (LSCB) and stem
wood (LSCS) – depended significantly (P  0.001) on canopy
position, but only two (kS, LSCS) were influenced by
humidification manipulation (Table 2). Branch morphological
traits also depended on canopy position (Table 1) and were
unaffected by the humidification treatment. Stem hydraulic
conductivity, kS, increased by 14–32% in response to
humidification, with the greatest increase in the lower stem
position (Fig. 2). LSCS and kS decreased in the stem apical
direction (Fig. 2), whereas branch hydraulic characteristics
tended to be greatest in the mid-canopy (Fig. 3), i.e. in the
layer with the largest branches. Neither branch-wood (rB) nor
stem-wood (rS) density was dependent on the treatment. Wood
density was inversely related to k in branches (R2 = 0.465,
P < 0.001; Fig. 4a), but not in stems (P = 0.586). Stem radial
growth rate (DDS) decreased in response to humidification
(mean  s.e. across all positions was 3.42  0.204 and
2.97  0.134 mm year–1 in control and humidified trees
respectively), while branch radial growth rate (DDB) was
unaffected by humidification. At the same time, kB increased
with DDB (R2 = 0.446, P < 0.001; Fig. 4b), but there was no
significant relationship between kS and DDS.
Anatomical traits of stem xylem
Most anatomical traits differed significantly (P < 0.001)
between stem and branch samples (except VG) and with

Table 4. Results of ANOVA for effects of the humidification treatment and canopy position on
anatomical traits
ns, not significant at P < 0.05

Dependent variable Effect Branch Stem

Significance Partial h2 Significance Partial h2
Dv (mm) Treatment ns – ns –
Canopy position P < 0.001 0.420 P < 0.001 0.383
Av (mm2) Treatment ns – ns –
Canopy position P < 0.001 0.370 P < 0.001 0.385
VG Treatment ns – ns –
Treatment
Canopy P = 0.027 0.143 ns –
Canopy position P < 0.001 0.366 ns –
VA (%) Treatment ns – P = 0.006 0.145
Canopy position ns – ns –
VD (mm–2) Treatment ns – ns –
Treatment
Canopy ns – P < 0.001 0.445
Canopy position P < 0.001 0.442 P = 0.030 0.094
Ivul (mm3) Treatment ns – P < 0.001 0.402
Canopy position P < 0.001 0.542 P < 0.001 0.578
Dh (mm) Treatment ns – ns –
Canopy position P < 0.001 0.384 P < 0.001 0.457
kt (kg m–1 s–1 MPa–1) Treatment ns – ns –
Canopy position P < 0.001 0.668 P = 0.011 0.165
H Functional Plant Biology A. K. Jasi

nska et al.

(a) Control Humidification

conductivity (kt; Fig. 8). Ivul was 51% greater in stem wood
20
Stem compared with branch samples. In stems Ivul was influenced by
Vessel relative area, VA (%)

b Treatment effect p = 0.006 humidification manipulation, but depended significantly on

18 b
canopy position in both stems and branches (Table 4). kt
b
depended on treatment, but in contrast to experimentally
16 a a
a measured specific hydraulic conductivity (kS), decreased with
increasing air humidity (Table 3). Results showed that kS was
14 related with neither kt nor most measured anatomical traits. VA in
stems depended more on vessel density (partial correlation
12 coefficient: 0.69–0.71) than on vessel size (Dv, Av; partial
correlation coefficient: 0.62–0.64), in contrast to kt (partial
10 correlation coefficients were 0.51–0.55 and 0.84–0.87
(b) respectively).
Stem
a Treatment effect p = 0.006 Pit membrane area (Apit) and pit aperture area (Aap)
250
Position effect p < 0.001 depended both on treatment and canopy position, and pit
Vessel density, VD (mm–2)

ab ab density (PD) only on position, whereas pitfield fraction (PF)

abc
was independent of both. The pit membrane and aperture areas
200 were greater in control plots than in misted plots (Table 5).
bc
c Humidification had no significant effect on PD and PF,
although both traits were greater in C plots (12443 mm–2,
150 70.5% respectively) than in H plots (12246 mm–2, 68.4%
respectively). Apit increased with vessel diameter (R2 = 0.162,
P = 0.003), indicating that wider vessels also have bigger
100 intervessel pits. Apit was negatively correlated with Aap and
PD. The acropetal increase in Aap and PD in stems means that
(c) wide vessels in the lower position have the greatest Apit, but the
2.0 Branch smallest aperture area and the lowest pit density. Experimentally
Vessel grouping index, VG

a Treatment* position effect p = 0.027

Position effect p < 0.001
1.9
ab
1.8
bc
1.7
1.6
1.5
Upper Medium
Canopy position
Fig. 5. Variation in stem vessel relative area (VA), stem vessel density
(VD) and branch vessel-grouping index (VG) with treatment and sample
position in control and humidified trees. Error bars indicate  s.e. of
the means; different letters denote statistically significant (P < 0.05)
differences.
canopy position (except VG for stems and relative area of
vessel lumina (VA) for stems and branches; Tables 3, 4). The
samples of humidity-treated trees were characterised by
decreased VA in stems (Fig. 5a): H – 15.0%, C – 16.7%
(P = 0.006). VA was positively correlated with vessel density
(VD; R2 = 0.19, P = 0.001). The lowest number of vessels per
unit area was recorded at the stem base (Fig. 5b), where the
vessel lumen area (Av) was greatest. Av decreased in stems with
height above the ground (R2 = 0.43, P = 0.006; Fig. 6).
The combined effect of misting treatment and canopy
position affected stem VD significantly (P < 0.001):
H – 184 mm–2, C – 203 mm–2. A decrease in vessel density in
both branches and stems is associated with an increase in mean
vessel diameter (Dh), accompanied by an increase in xylem
vulnerability index (Ivul; Fig. 7) and theoretical specific
measured specific hydraulic conductivity (kS) was negatively
correlated with PD, Aap and PF (Pearson correlation
coefficients were –0.27, –0.29 and –0.36 respectively).
bc
c Anatomical traits of branch xylem
c
The mean area of vessel lumina in branches was half that in
stems (Table 3). Av in branches increased with height above the
Lower ground (R2 = 0.30, P < 0.001), in contrast to stems (Fig. 6). Av
was strongly correlated with branch diameter (Pearson
correlation coefficient: 0.99). Only one wood trait in branches
was affected by humidification: vessel-grouping index (VG, H –
1.70, C – 1.67) depended on the interactive effects of treatment
and canopy position (P = 0.027; Fig. 5). VG was positively
correlated with hydraulic traits kt and kB, and negatively with
wood density (rB; P < 0.05). As experimentally measured
specific conductivity of branch wood (kB) increased with
increasing Dv and VA (Fig. 9), a fair correlation (R2 = 0.412,
P < 0.001) between the empirical and theoretical values of k was
observed. Variation in both VA and kt in branches was driven
by changes in vessel dimensions (Dv, Dh, Av) and was
independent of VD; the partial correlation coefficients for VA
and kt were in the range 0.28–0.30 and 0.72–0.79 respectively.
The combination of VA, a quantitative measure of the water-
conducting surface, and Dh, a qualitative characteristic of the
water-conducting surface, accounted for 87.4% of the total
variation in kt in branches and 85.5% of that in stems across
the treatments (Fig. 10). Although VA exhibited higher
plasticity (PI: 0.53 for branches and 0.48 for stems) than Dh
(PI: 0.47 for branches and 0.37 for stems), variation in kt was
associated with Dh rather than with VA (partial correlation
coefficients: 0.92 and 0.77 respectively.
Air humidity affects hybrid aspen xylem traits Functional Plant Biology I

2000

Branch C
Branch H
1700 Stem C
Stem H

Vessel lumen area, A v (µm2)

1400
R 2 = 0.4338
p = 0.006

1100

800

500

R 2 = 0.3036
p < 0.001
200
0 100 200 300 400 500
Height above the ground surface, H (cm)

Fig. 6. Vessel lumen area (AV) in relation to height above the ground surface (H); C, control;
H, humidification.

46 0.55

Dh (R 2 = 0.21, p < 0.001)

0.50
Ivul (R 2 = 0.83, p < 0.001)
Hydraulically weighted mean diameter, Dh (µm)

44

0.45

Xylem vulnerability index, Ivul (µm3)

42
0.40

40 0.35

38 0.30

0.25
36
0.20

34
0.15

32 0.10
80 100 120 140 160 180 200 220 240 260 280

Vessel density, VD (mm–2)

Fig. 7. Inverse relationship between stem hydraulically weighted mean diameter (Dh), xylem
vulnerability index (Ivul) and vessel density (VD).

Discussion the reduced atmospheric evaporative demand (AED) due to

the misting application resulted in greater than half lower
Impact of air humidity sap flux densities in 2009 and a lesser decrease in the
Artificially elevated air humidity (long-term mean RH following years (Kupper et al. 2011). It is probable that the
increased by 7%; Kupper et al. 2011) had no impact on water fluxes through the branches are so much smaller and
hydraulic property or anatomical traits (except for VG) the structure of branch wood more constant, so the humidity
measured in hybrid aspen branches. At the whole-tree level, manipulation did not cause significant effects.
J Functional Plant Biology A. K. Jasi

nska et al.

Unlike branch wood, the humidity manipulation
influenced both theoretical specific conductivity (kt) and
specific hydraulic conductivity, measured experimentally in
stem segments (kS). However, the results were unexpected: kS
increased (Fig. 2), whereas kt showed a decreasing trend in
response to elevated RH. Although mean values of kS did not
differ in any stem position when analysed separately, the
treatment effect on the whole dataset was highly significant
(P = 0.003). We note that kS was determined on cut wood
segments by applying the high-pressure method, which may
overestimate hydraulic parameters compared with those
measured in intact plants. The trends in these traits should
concur, although absolute values of kt are usually higher than
measured values (Tyree and Zimmermann 1971; Lovisolo and
Schubert 1998). Theoretical specific conductivity was calculated
only from vessel diameter and vessel density data. However, real
hydraulic conductivity depends on several anatomical
characteristics, including vessel length, secondary cell wall
thickening, and density and structure of intervessel pits. We
discovered that the size of intervessel pits depends on the
experimental manipulation (Table 5), but PD, Aap and PF were
inversely correlated with kS. Thus, the discrepancy between kS
and kt cannot be attributed to size or frequency of bordered pits.
However, Aumann and Ford (2006) indicated that lower
bordered pit density may enhance kS under certain conditions.
These authors proved that the benefits of increasing PD depend
on meteorological conditions – in dry environments, wood
with fewer pits is more conductive over time than wood with
Our study revealed that increasing atmospheric humidity
decreases VD in aspen stem wood (Fig. 5b). Because the air
humidity manipulation did not affect vessel diameter (Dv, Dh), kt
was less in trees growing on H plots, although we established
an inverse relationship between Dh and VD (Fig. 7). Also, an
increasing proportion of parenchyma in stems of trees grown
under high air humidity may contribute to the observed reduction
of VD (Tullus et al. 2014). Elevated atmospheric humidity also
has a negative impact on the development of the leaf vascular
system: birch saplings from H plots exhibited considerably
smaller Dv (P = 0.025), Dh (P = 0.018), lower kt (P = 0.006) in
midvein and lower vein frequency (P = 0.064) than the control
(Sellin and Alber 2013).
Preston et al. (2006) suggested that it is not merely a simple
compromise between size and number of vessels to keep wood
density fairly constant, but that this inverse relationship
has ecological consequences. Sellin et al. (2008) described the
strong negative correlation between vessel diameter and density
(Fig. 7) as a basic trade-off between hydraulic efficiency and the
mechanical stability of xylem. Maintaining relatively constant
wood density cannot itself be a target of natural selection or
pressure of ecological drivers. The function of certain anatomical
structures can be to maintain sufficient mechanical strength
and stem stability; this is achieved not only by decreasing
vessel density (more fibres), but also by other means, e.g.
thicker cell walls of fibres and vessels, larger stem or branch
Theoretical specific conductivity, kt

16
more pits. Branch C R 2 = 0.6817
Some relevant but unmeasured traits (e.g. pit membrane pore Branch H p < 0.001
(kg m–1 s–1 MPa–1)

size, vessel length, cell wall secondary thickening) changed to a 12 Stem C

Stem H
greater degree as a result of humidification, causing the
opposite shifts in kS with respect to kt. Thus, our results
8
suggest that declined water fluxes through the trees due to
lower AED do not necessarily induce a decrease in their R 2 = 0.6324
p = 0.003
hydraulic capacity. In B. pendula, another species in the 4
FAHM experiment, hydraulic traits responded differently to
humidity manipulation: leaf hydraulic conductance (KL)
0
decreased, whereas hydraulic conductance of root systems and 20 30 40 50 60
LSCS increased in response to elevated RH (Sellin et al. Hydraulically weigthted mean diameter, Dh (um)
2013). The reasons for the opposite trends in theoretical and
experimentally measured hydraulic conductivity of aspen stem Fig. 8. Hydraulically-weighted mean diameter (Dh) versus theoretical
wood need further anatomical studies. specific conductivity (kt).

Table 5. Comparison of pit characteristics (mean þ s.e.) and results of ANOVA for effects of the humidification
treatment and canopy position on pit traits
ns, not significant

Characteristic Control Humidification Effect Significance Partial h2

Pit area, Apit (mm2) 58.3 ± 0.5 56.8 ± 0.5 Treatment P = 0.022 0.005
Canopy position P < 0.001 0.118
Pit aperture area, Aap (mm2) 6.10 ± 0.1 5.80 ± 0.1 Treatment P = 0.032 0.004
Canopy position P < 0.001 0.078
Pit density, PD (mm–2) 12443 ± 267 12246 ± 249 Treatment ns –
Canopy position P < 0.001 0.155
Pitfield fraction, PF (%) 70.6 ± 2.3 68.3 ± 1.9 Treatment ns –
Canopy position ns –
Air humidity affects hybrid aspen xylem traits Functional Plant Biology K

diameter and changes in cell wall ultrastructure (density and trait (varied in a wider range), variation in kt was primarily
orientation of cellulose fibrils). In contrast, the structure of the driven by vessel diameter. This suggests that conduit size
water-conducting system should allow adequate water distribution rather than total conducting area (i.e. total cross-
supply to foliage in order to keep stomata open and to achieve sectional area of vessel lumina) determines xylem hydraulic
a positive carbon budget under changing environmental efficiency in hybrid aspen. In addition, the hydraulic
conditions. measurements support this conclusion: kB was more strongly
Further, the changes observed in anatomical traits of stem related to Dv than VA (Fig. 9). VA and Dh combined accounted
xylem (Table 3) in response to elevated atmospheric humidity for 86–87% of the total variation of kt in hybrid aspen (Fig. 10).
are logical and can be attributed to reduced transpirational Humid conditions should lead to higher xylem functional
water fluxes (Kupper et al. 2011; Tullus et al. 2012) caused by vulnerability, making plants more susceptible to environmental
lower AED. In addition, vessel lumen area demonstrated a fluctuations (Barigah et al. 2013). Our results indicate that
decreasing trend in the H treatment, although the changes were vessel density decreased with increasing RH, which may
not statistically significant because of high data dispersal. The adversely affect xylem vulnerability (Ivul increased; Fig. 7).
tendency of vessel size to decrease in stems of humidity-treated However, the changes in Ivul were too small for the treatment
trees is in accordance with their decreased radial growth rate, a effect to be statistically significant (Tables 3 and 4). The
relationship proved in both intra- and interspecific studies (Fan experimental estimation of xylem vulnerability to cavitation in
et al. 2012). Aspen trees grown at the FAHM site under elevated
air humidity exhibited significantly reduced height, stem
diameter and stem volume increments (Tullus et al. 2012).
Increased air humidity impairs nitrogen uptake from soil and (a)
foliar nutrient status, inducing negative consequences on leaf
photosynthetic capacity. For fast-growing taxa, such as hybrid 7.5
aspen that are bred for intensive forestry, this results in
considerable growth retardation. The same consequences were kt (kg m–1 s–1 MPa–1)
6.0
encountered in saplings of silver birch grown under elevated
RH (Sellin et al. 2013). Although VA was the more plastic
4.5

3.0
(a) R 2 = 0.502, P < 0.001
Control
20
Humidification
20
18
Specific conductivity of branchwood, kB (kg m–1 s–1 MPa–1)

15 44
16 40
VA 14 36
(% 12 32 )
10 )
10 28 (µm
Dh
8 24

5 (b)

0 14
20 22 24 26 28 30
Mean vessel diameter, Dv (µm)
kt (kg m–1 s–1 MPa–1)

12

10
(b) R 2 = 0.201, P = 0.006
20 8

6
15
4

10 22
20 56
52
18
5 VA 48
(% 16 )
) 44 (µm
14 40 Dh
0 12
8 10 12 14 16 18 20
Vessel relative area, VA (%) Fig. 10. Theoretical specific conductivity of xylem (kt) as a function of
mean hydraulic diameter of vessels (Dh) and vessel relative area (VA)
Fig. 9. Variation in specific conductivity of branch wood (kB) depending in branch wood (a, R2 = 0.874, P < 0.001) and stem wood (b, R2 = 0.855,
on mean vessel diameter (a, Dv) and relative vessel area (b, VA). P < 0.001).
L Functional Plant Biology
aspen coppice shoots did not reveal any influence of increased
RH (A Sellin, unpubl. data). Our results suggest that changes in
atmospheric humidity applied in the present study (long-term
RH +7%) have no substantial effect on xylem functional
vulnerability.
Variation with canopy position
The results demonstrated that the vessels were significantly
larger (i.e. vessel lumen diameter and area) in stem wood than
in branch wood (Table 3). The observed difference and numerical
values of the traits measured in hybrid aspen saplings are
comparable to those reported in the literature (Castro-Diez
et al. 1998; De Micco et al. 2008; Plavcova and Hacke 2012).
All these studies confirm that the water-conducting system in
branches is hydraulically less efficient than that in stems.
However, branches are hydraulically much safer because
vessels are more grouped than in stems (De Micco et al. 2008;
McCulloh et al. 2014). Our data on Ivul in aspen stems versus
branches confirm this trend, although the index is not associated
with the vessel-grouping index (VG) in stems. Ivul increases with
vessel size and is inversely related to vessel density (Fig. 7) and
being strongly affected by canopy position. Ivul of branches
decreased downwards in the canopy: the greatest values in
stems were found in the mid-position. The capability of xylem
to withstand water stress, as well as the efficiency and safety of
the hydraulic system, depends not only on the size and number
of vessels, but also on structural traits of the cell wall, pit
membranes and the relationships among different wood
elements, including vessels, fibres and parenchyma rays
(Sperry et al. 2006). Our branch samples exhibited higher
wood density (rB), a trait usually associated with greater
hydraulic safety (Fan et al. 2012).
Numerous papers have indicated that the traits associated
with water transport capacity in various tree species tend to
decrease basipetally in the canopy (Sellin and Kupper 2004,
2005). This pattern is thought to promote the hydraulic
dominance of upper-canopy branches over the lower shaded
branches; in this way, crown architecture contributes to
preferential water flow along the main axes, potentially
providing a better water supply to foliage located in the upper,
better insolated part of the crown. It is an important prerequisite
in tall forest trees that experience considerable within-canopy
environmental gradients to support higher stomatal conductance
and transpiration rates in sun-exposed foliage, which is
photosynthetically the most important part of the canopy
(Sellin et al. 2010). In stems of aspen saplings, we observed
opposite trends: hydraulic conductivity (kS and LSCS; Fig. 2) and
vessel lumen area (Av; Fig. 6) tended to increase in the basipetal
direction. This result is in accordance with the distally tapering
pattern of xylem conduits, a strategy that should reduce the
effect of height on the total path-length resistance and
minimise the tree-level hydrodynamic resistance of water
transport from roots to leaves (Bettiati et al. 2012; Anfodillo
et al. 2013).
In branches of hybrid aspen saplings, we rather observed
another pattern: the structural (Av, HVB) characteristics
increased in the upward direction (Table 1; Fig. 6), while the
hydraulic efficiency (kB and KB) was greatest in the medium
A. K. Jasi

nska et al.
canopy layer (Fig. 3). The latter can be attributed to significant
differences in branch morphology (Table 1): the large leaf area
and small Huber value in branches in the medium canopy layer
are compensated by higher hydraulic efficiency to provide
adequate water delivery to the foliage. In small saplings, the
within-canopy vertical trends are evidently not so well
pronounced because their branches are younger and the
distances between them shorter than in tall forest trees.
Conclusions
Our results suggest that increasing atmospheric humidity –
a climate trend predicted for high latitudes – will induce
moderate changes in xylem structure of hybrid aspen, which
will probably not impair its water transport capacity. We found
that, regardless of size effects (tree height, sample diameter),
increased humidity reduces the area occupied by vessels, their
density and size of intervessel pits in stem wood. Stem wood,
which supports greater transpirational fluxes, is more susceptible
to environmental changes compared with branch wood, as
substantiated by both anatomical and hydraulic traits.
Humidity manipulation affected both experimentally measured
(kS) and theoretical values (kt) of stem-wood hydraulic
conductivity, although in opposite directions, and this issue
requires further research. Canopy position has a considerable
impact on wood anatomy of hybrid aspen, influencing most
traits of branch and stem wood. The diverse spatial patterns of
structural and functional characteristics within branches versus
stems likely reflect a compromise between the vessel apical
tapering pattern to reduce the total path-length resistance and
within-crown water requirements associated with vertical
distribution of foliage.
Acknowledgements
This work was supported by the EU through the European Social Fund
(Mobilitas postdoctoral grant numbers MJD398, MJD257) and through
the European Regional Development Fund (Centre of Excellence in
Environmental Adaptation), by the Estonian Science Foundation (Grant
no. 8333) and by the Estonian Ministry of Education and Research
(institutional research funding IUT 34-9). We thank Jaak Sõber for
operating the FAHM misting system and Robert Szava-Kovats for
language revision.
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