Research
Drought-induced xylem cavitation and hydraulic deterioration:
risk factors for urban trees under climate change?
Tadeja Savi, Stefano Bertuzzi, Salvatore Branca, Mauro Tretiach and Andrea Nardini
Dipartimento di Scienze della Vita, Universita di Trieste, Via L. Giorgieri 10, Trieste 34127, Italy
Summary
Author for correspondence:
Andrea Nardini
Tel: +39 040 5583890
Email: nardini@units.it
Received: 23 July 2014
Accepted: 14 September 2014
New Phytologist (2015) 205: 1106–1116
doi: 10.1111/nph.13112
Key words: climate change, dieback,
embolism, hydraulic deterioration, Quercus
ilex, towns, urban trees, xylem vulnerability.
Urban trees help towns to cope with climate warming by cooling both air and surfaces. The
challenges imposed by the urban environment, with special reference to low water availability
due to the presence of extensive pavements, result in high rates of mortality of street trees,
that can be increased by climatic extremes.
We investigated the water relations and xylem hydraulic safety/efficiency of Quercus ilex
trees growing at urban sites with different percentages of surrounding impervious pavements.
Seasonal changes of plant water potential and gas exchange, vulnerability to cavitation and
embolism level, and morpho-anatomical traits were measured.
We found patterns of increasing water stress and vulnerability to drought at increasing
percentages of impervious pavement cover, with a consequent reduction in gas exchange
rates, decreased safety margins toward embolism development, and increased vulnerability to
cavitation, suggesting the occurrence of stress-induced hydraulic deterioration.
The amount of impermeable surface and chronic exposure to water stress influence the
site-specific risk of drought-induced dieback of urban trees under extreme drought. Besides
providing directions for management of green spaces in towns, our data suggest that xylem
hydraulics is key to a full understanding of the responses of urban trees to global change.
Introduction
Ongoing climate changes are increasing the frequency of drought
and heatwaves in several areas of the globe (Prudhomme et al.,
2014), and urbanized areas will be likely hotspots of temperature
rise, as a consequence of the ‘urban heat island’ effect (Oleson
et al., 2011). Increasing temperatures in towns are predicted to
imply significant economic and social costs over coming decades
(Scheraga & Grambsch, 1998; Luber & McGeehin, 2008), thus
calling for the adoption of mitigation and adaptation strategies
by local municipalities and national governments.
Urban trees represent effective tools to improve urban climate
(Bowler et al., 2010; Sung, 2013), as they effectively cool down
air and surfaces (Armson et al., 2012; Sung, 2013) through shading
effects and evaporative processes (Pataki et al., 2011). However,
the effectiveness of ecosystem services provided by trees can be
impaired by canopy dieback induced by abiotic (Vilagrosa et al.,
2003) and biotic stress factors (Nardini et al., 2004; Meineke
et al., 2013), or as a consequence of prolonged stomatal closure
induced by water stress (Bush et al., 2008; Litvak et al., 2012).
Hence, the success of urban forestry as a mitigation strategy
against climate warming depends on the health status of trees,
which in turn has important consequences for the health of people
living in towns (Villeneuve et al., 2012; Donovan et al., 2013).
Over the last decades, episodes of tree decline triggered by
drought and heatwaves have been reported for different
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ecosystems (Allen et al., 2010; Michaelian et al., 2011; Peng
et al., 2011). The physiological bases of drought-induced tree
decline are still unresolved and likely involve at least three functional levels: water transport, carbon metabolism and plant
responses to biotic agents (McDowell et al., 2011, 2013). The
drought-induced reduction of plant water potential can lead to
massive xylem cavitation and impairment of root-to-leaf water
transport, thus leading to plant desiccation (Breshears et al.,
2013; Nardini et al., 2013; Mitchell et al., 2014). In turn, prolonged stomatal closure caused by reduced water transport capacity, or addressed at preventing xylem pressure drop (Salleo et al.,
2000), can lead to depletion of nonstructural carbohydrate
reserves (Adams et al., 2013; Poyatos et al., 2013; Sevanto et al.,
2014). Finally, carbon starvation might lead to impairment of
plants’ defense strategies against biotic agents (Rivas-Ubach et al.,
2014), favoring heavy attacks by different pests (McDowell,
2011; Anderegg & Callaway, 2012; Gaylord et al., 2013).
Whatever the exact mechanism leading to tree decline, there is
general consensus around the crucial role played by vulnerability
to xylem cavitation in driving plants’ responses to extreme climatic events (Rice et al., 2004; Brodribb & Cochard, 2009;
Choat et al., 2012). Hence, it is not surprising that several studies
have investigated the correlations between tree hydraulics and
drought performance in natural habitats (Pratt et al., 2008; Hoffmann et al., 2011; Nardini et al., 2013). However, the hydraulics
of urban trees has only rarely been considered as a possible
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vulnerability factor modulating the risk of canopy dieback under
environmental stress (Bush et al., 2008; Litvak et al., 2012).
The challenges imposed by the urban environment on plant
functioning result in high rates of drought-induced mortality of
street trees (Nowak et al., 2004; Roman et al., 2014), that can be
exacerbated by climatic extremes (Helama et al., 2012; May et al.,
2013). Urban trees can be exposed to significant water stress
because of high air temperatures and reduced water availability
(Gillner et al., 2013). In particular, water supply to urban trees is
complicated by soil compaction (Yang & Zhang, 2011) and by
extensive impervious surfaces preventing or delaying recharge of
soil water content following rainfall events (Morgenroth et al.,
2013). These factors can also reduce root growth and vitality via
mechanical effects (Day et al., 2010) or by altering gas diffusion
through the rhizosphere (Viswanathan et al., 2011) with predictable chronic water restrictions for trees growing in areas with
compacted and/or impervious soils (Ugolini et al., 2012). On the
one hand, chronic exposure to moderate water stress might drive
acclimation responses of the tree hydraulic system in terms of
efficiency and safety (Awad et al., 2010; Wortemann et al.,
2011), making urban trees less susceptible to extreme events. On
the other hand, long-term water stress experienced by trees growing in less favorable spots in terms of water availability, might
actually drive the progressive hydraulic deterioration of the xylem
system via ‘cavitation fatigue’ (Hacke et al., 2001) processes,
as recently shown for poplar (Anderegg et al., 2013) and ash
(Nardini et al., 2014), thus increasing the vulnerability of trees to
successive drought events.
We specifically addressed these questions by comparing the
water relations and xylem hydraulic safety/efficiency of Quercus
ilex (holm oak) trees growing in urban sites characterized by different levels of impermeability of surrounding soil. We specifically tested the following hypotheses: trees growing in areas
characterized by extensive impervious surfaces experience more
intense seasonal water stress than those growing in areas with permeable surfaces; water stress translates into higher levels of embolism and reduced gas exchange rates; chronic water stress leads to
increased vulnerability to xylem cavitation and hydraulic deterioration (Anderegg et al., 2013) in trees growing in areas with
extensive impervious surfaces.
Materials and Methods
Study sites and plant material
Experiments were conducted in the urban area of Trieste, Italy, a
middle-sized town (210 000 inhabitants) on the Adriatic coast,
and spreading over a substrate of Eocenic Flysch deposits (Onofri, 1982). The climate of Trieste is transitional between the
Mediterranean and Central European types, with equinoctial
rainfalls, cold winters and relatively dry periods in December–
February and July–August (Codogno & Furlanetto, 2004). The
mean annual temperature averages 14.4°C, and annual rainfall
totals 1065 mm (http://www.meteo.fvg.it). Approximately 4% of
the urban zone is covered by green areas in which Mediterranean
tree species are often used as ornamental plants. The species
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Research 1107
Fig. 1 Location of the four experimental sites along the coastline of the
Municipality of Trieste (northeastern Italy). The percentages of
surrounding soil surface cover with pervious (green) or impervious
pavement (gray) are reported (see the Materials and Methods section for
details).
selected for the study is Quercus ilex L. (holm oak) due to its
widespread presence in Trieste and availability of previous studies
focused on its water relations (Tretiach, 1993; Nardini et al.,
2000). Four sites were selected along a NW–SE transect parallel
to the coastal line (Fig. 1), on the basis of the presence of at least
three adult individuals of Q. ilex and different percentages of soil
coverage with impervious substrates. The percentage of paved
surface at each site was quantified in a circular area centered on
experimental trees and with a radius of 25 m, for a total surface
of c. 2000 m2. Spatial analysis was performed on Google Earth
images (http://www.google.com/earth) processed using ImageJ
(http://rsbweb.nih.gov/ij), and confirmed by direct field surveys.
At all sites, unpaved soil was covered by grass or small shrubs and
was apparently not subjected to significant compaction.
All selected trees were > 20-yr old, with a height between 6
and 10 m. Experimental measurements were performed on three
individuals per site between June and September 2013. Climatic
data (air temperature and relative humidity) were continuously
recorded (at 30-min intervals) throughout the study period by
EL-USB-2 dataloggers (Laskar Electronics Inc., Salisbury, UK)
positioned at a height of 3 m on the north-facing side of the main
trunks of two individuals per site. The study period was characterized by abundant rainfall in May–June (202 mm) and a dry
period in July–August (55 mm), interrupted in early September
(10 d before the last seasonal measurements) by late-summer
thunderstorms accumulating a total rainfall of 97 mm.
Measurements of leaf gas exchange rates and plant water
status
The leaf conductance to water vapor and water potential were
measured on a monthly basis on fully expanded current-year
leaves, sampled from the outer portion of the south-facing canopy. Pre-dawn leaf water potential (Ψpd) was measured between
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05:00 and 06:00 h (solar time). Two leaves per individual (six
leaves per site) were collected and immediately wrapped in clingfilm, stored in a refrigerated bag and transported to the laboratory within 30 min. Water potential was measured using a
pressure chamber (mod. 1505D; PMS Instrument Company,
Albany, OR, USA). The sampling was repeated on the same day
between 11:00 and 13:00 h, to estimate minimum daily leaf
water potential (Ψmin). Minimum xylem water potential (Ψxyl)
was also estimated by measuring the water potential of leaves that
had been covered with clingfilm and aluminum foil at pre-dawn,
to allow equilibration of leaf water potential with xylem pressures. On the day following Ψ measurements, leaf conductance
to water vapor (gL) was measured between 11:00 and 13:00 h.
Measurements were performed on two leaves per individual (six
leaves per site) using a steady-state porometer (SC-1; Decagon
Devices Inc., Pullman, WA, USA). All measurements were performed on clear sunny days with PPFD ranging between 700 and
1600 lmol m 2 s 1.
Measurements of photosynthetic efficiency
On the same dates and times when gL was measured, the photosynthetic efficiency was estimated by Chlorophyll a Fluorescence
(ChlaF) emission measurements, performed on three leaves per
individual (nine leaves per site) selected as detailed above and
darkened 20 min before measurements. Measurements were done
with a portable fluorometer (Handy Pea; Hansatech, Norfolk,
UK), and Fv/Fm was calculated as a proxy for quantum yield of
PSII (Maxwell & Johnson, 2000).
Measurements of xylem vulnerability to cavitation and
percentage loss of stem hydraulic conductivity
In order to assess site-specific tree vulnerability to droughtinduced xylem cavitation, vulnerability curves (VCs) were measured for 2-yr-old stems using the bench dehydration technique
(Cochard et al., 2013). Measurements were performed in July
2013, after the May–June rainy period and before the onset of
substantial water stress. Five-year-old branches (randomly selected
from the three individuals in each site) were cut underwater in
the field between 07:00 and 08:00 h. Branches were transported
to the laboratory and kept with their cut ends immersed in water
and with foliage enclosed in a plastic bag for 24 h. This procedure
favored full branch rehydration and refilling of eventually embolized conduits (Trifilo et al., 2014a). Branches were removed from
water and dehydrated on the bench at laboratory irradiance, temperatures ranging between 20 and 22°C, and relative humidity
averaging 45%. At 60–90-min intervals, Ψxyl was measured in
wrapped leaves. Hydraulic measurements were performed on 20–
22 samples at different Ψxyl (between 0 and 3.5 MPa). Twoyear-old stems were recut underwater to a length of 5–7 cm, connected to an hydraulic apparatus (Xyl’Em – Xylem Embolism
Meter; Bronkhorst, Montigny-les-Cormeilles, France) and perfused with a commercial mineral water containing several elements in ionic form and with K+ adjusted to 10 mM (Nardini
et al., 2011). The solution was initially perfused through stems at
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a pressure (P) of 8 kPa until the flow (F) became stable (within
10–12 min). Stems were then flushed at P = 0.2 MPa for 15 min
to remove embolism and flow was re-measured at P = 8 kPa.
Stem hydraulic conductivity (K) was computed as (F/P) 9l (l,
stem length. The initial K (Ki) and the value measured after
embolism removal (Kmax) were used to estimate the percentage
loss of stem hydraulic conductivity (PLC) as:
PLC ¼ 1
ðKi =Kmax Þ 100
(1)
In order to assess the impact of seasonal water stress on xylem
functioning, midday PLC values experienced by plants were measured on a monthly basis, in the same weeks when Ψ and gL measurements were performed. Two-year-old stems (two per
individual, six stems per site) were cut underwater in the field
between 11:00 and 13:00 h, and transported to the laboratory
within 30 min, while remaining immersed in water. Samples
were re-cut underwater to a length of 5–7 cm and their PLC was
measured as described above. Upon sampling in the field, Ψxyl
was measured as described above.
In August, when maximum seasonal PLC was recorded at all
sites (see the Results section), all leaves inserted distally to the
stem segments used for hydraulic analysis were detached, and
total surface area (Aleaf) was measured by scanning leaves and
analysing images with ImageJ. Leaf specific hydraulic conductivity of stems (LSC) was calculated as K/Aleaf, and using both Ki
and Kmax values, thus getting LSCi and LSCmax.
Morpho-anatomical measurements
Wood density and vessel size were measured for a sub-set of stems
used for hydraulic measurements (15 samples per site). Two-centimeter-long samples were fully rehydrated overnight while
immersed in distilled water. After bark removal, their fresh volume was measured by water displacement (Hughes, 2005). Samples were oven-dried for 24 h at 70°C to determine their dry
mass. Wood density (dw) was calculated as dry mass/fresh volume
(Markesteijn et al., 2011). Stem cross-sections (three per individual, nine samples per site) were obtained using a microtome and
immediately observed under a light microscope. Images were
acquired using a digital camera and analyzed with ImageJ. Xylem
conduit diameters were measured on at least 20–30 randomly
selected elements per section.
Statistics
Statistical analysis was performed using SigmaStat v2.0 (Systat,
San Jose, CA, USA). The significance of differences was tested
using one-way ANOVA followed by Tukey’s post-hoc comparisons. The significance of correlations was tested using the Pearson
product-moment coefficient.
Results
The four study sites differed in terms of percentage paved soil
surface. In the Miramare (S45) and Scala (S52) sites, < 50% of the
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45
Roiano, S80
35
Tmax (°C)
600
Miramare, S45
Scala, S52
40
500
Barcola, S90
gL (mmol s–1 m–2)
30
25
20
15
10
140
160
180
200
220
240
260
280
RH (%)
Miramare, S45
Scala, S52
Roiano, S80
Barcola, S90
100
June
60
July
August
September
Fig. 3 Seasonal changes of leaf conductance to water vapor (gL) as
measured in Quercus ilex trees growing at four experimental sites with
different percentages of soil surface pervious or impervious pavement
cover (see Fig. 1). Means are reported SEM. Significant differences
between sites (one-way ANOVA): *, P < 0.05.
40
20
160
180
200
220
240
260
160
180
200
220
240
260
280
300
280
300
5
4
VPD (kPa)
300
200
80
3
2
1
0
140
*
400
300
100
0
140
*
June 1st
Day 152
Julian days
October 1st
Day 274
Fig. 2 Seasonal trend of daily maximum air temperatures (Tmax), minimum
relative humidity (RH) and vapor pressure deficit (VPD) as measured at the
four study sites. Each point represents the mean of values recorded by two
sensors located at each site (see Materials and Methods section for
details).
soil surface was impermeable, increasing to 80% and 90% in
Roiano (S80) and Barcola (S90), respectively (Fig. 1). In addition,
sites S80 and S90 had higher air temperatures and lower relative
humidity than the other sites (Fig. 2). For example, in early
August air temperatures in S90 peaked at 40°C, but were 7–9°C
lower in S45 and S52. The maximum daily vapor pressure deficit
(VPD) was 0.5–2 kPa higher in S90 and S80 than in S45 and S52;
the mean of maximum daily VPD values recorded from early
June to mid-September were 1.59 0.74, 1.70 0.71,
1.75 0.73 and 2.15 0.93 kPa in S45, S52, S80 and S90, respectively.
In June, after a prolonged rainy period, gL averaged
450 mmol s 1 m 2, with peaks up to 700 mmol s 1 m 2 in S45
(Fig. 3). These values remained substantially stable in July, at the
early onset of summer drought, but decreased significantly in
August, when gL averaged 320 mmol s 1 m 2 across sites. In September, following late-summer rainfall, gL recovered in the sites
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with the lowest percentage of impervious surface (S45 and S52),
where it returned to 397 33 and 382 24 mmol s 1 m 2,
respectively. However, a further gL drop was observed in S80 and
S90 (200 23 and 259 43 mmol s 1 m 2, respectively).
In June, Ψpd ranged between 0.1 and 0.6 MPa in S45 and
S90, respectively (Fig. 4). A slight seasonal Ψpd decrease was
observed in all study sites, but this was much more abrupt in S90
in August, when Ψpd dropped to c. 1.2 MPa, whereas in the
other sites it ranged between 0.4 and 0.6 MPa. Both Ψmin
and Ψxyl were found to be significantly higher throughout the
season in S45 and S52 than in S80 and S90. Absolute minimum
values of Ψmin and Ψxyl were recorded in S90 in August
( 2.5 0.3 and 2.0 0.3 MPa, respectively), whereas trees
growing in S52 experienced the lowest level of water stress, with
Ψmin and Ψxyl averaging 1.0 0.2 and 0.5 0.1 MPa,
respectively (Fig. 4). Leaf water potential increased after the September rainfall, but the magnitude of the recovery varied among
sites. As an example, in S45 Ψxyl increased from 1.6 MPa in
August to 0.7 MPa in September, whereas in S90 Ψxyl changed
only from 2.0 to 1.8 MPa in the same time interval. A clear
correlation emerged between gL and Ψmin, both within sites on a
seasonal basis and across sites in each study period. Fig. 5 reports
the correlation between these parameters across all sites and study
periods.
Table 1 reports values of Fv/Fm measured in August, at the
peak of seasonal water stress. Significant differences were
recorded among sites, with S45 and S52 displaying the highest Fv/
Fm (c. 0.82) and progressively lower values recorded in S80 (c.
0.79) and S90 (c. 0.77). Slightly significant differences were
observed in terms of wood density and xylem conduit dimensions
(Table 1), but no specific trend could be observed in relation to
the percentage of impervious surface surrounding trees, nor to
the level of water stress suffered by individuals.
Measurements of seasonal PLC progression revealed marked
differences between the study sites (Fig. 6a). Embolism levels
were constantly low throughout the season in S45 and S52, where
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–0.2
550
*
500
*
Ψpd (MPa)
–0.4
–0.6
*
–0.8
–1.0
gL (mmol m–2 s–1)
0.0
Scala, S52
400
350
300
250
150
–2.6 –2.4 –2.2 –2.0 –1.8 –1.6 –1.4 –1.2 –1.0
Roiano, S80
–1.4
450
200
Miramare, S45
–1.2
r 2 = 0.76
P < 0.001
Barcola, S90
Ψmin (MPa)
–1.6
–0.8
–1.0
*
*
–1.2
Ψmin (MPa)
–1.4
–1.6
*
–1.8
*
Fig. 5 Relationship between leaf conductance to water vapor (gL) and
minimum daily leaf water potential (Ψmin) as measured throughout the
season (June–September) in Quercus ilex trees growing at four
experimental sites with different percentages of soil surface pervious or
impervious pavement cover (see Fig. 1). Each point represents the mean
value SD. The regression line together with r2 and P values is also
reported.
Table 1 Wood density (dw), xylem conduit diameter (Dv) and chlorophyll
fluorescence (Fv/Fm) as measured in Quercus ilex trees growing at four different urban sites with different percentages of impermeable surface cover
(see Fig. 1)
–2.0
–2.2
–2.4
–2.6
–2.8
–0.4
–0.6
*
Ψxyl (MPa)
–0.8
*
*
–1.0
*
–1.6
–1.8
–2.0
–2.2
June
July
August
September
Fig. 4 Seasonal changes of predawn leaf water potential (Ψpd), and
minimum daily leaf (Ψmin) and xylem (Ψxyl) water potential as measured in
Quercus ilex trees growing at four experimental sites with different
percentages of soil surface pervious or impervious pavement cover (see
Fig. 1). Means are reported SEM. Significant differences between sites
(one-way ANOVA): *, P < 0.05.
PLC ranged between 25% and 40%. In S80, low PLC (c. 20%)
was recorded in May, but this value sharply increased upon onset
of drought stress, reaching values as high as 70% in August.
Embolism was only partially reversed in September, when PLC
decreased to c. 50%. In S90, PLC was 55% in June, already, and
further increased to 70% in August. No recovery of PLC following late-summer rains was observed at this site.
In August, LSCi was similar across individuals (Fig. 6b),
despite marked differences in terms of PLC. When the same
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Dv (mm)
Fv/Fm
0.82 0.02 ab
0.77 0.05 a
0.87 0.03 b
0.84 0.06 ab
33.5 5.1 ab
37.1 7.0 a
33.4 4.8 ab
32.3 5.0 b
0.820 0.008 a
0.816 0.007 a
0.794 0.015 ab
0.765 0.033 b
Means are reported SD. Different letters indicate statistically significant
differences between sites (P < 0.05).
–1.2
–1.4
Miramare (S45)
Scala (S52)
Roiano (S80)
Barcola (S90)
dw (g cm 3)
parameter was calculated on the basis of maximum stem hydraulic conductivity measured after embolism removal, very similar
values were recorded at S45, S52 and S80, but at S90 the LSCmax
was significantly higher. This trend was driven by differences in
total leaf surface area supplied by 2-yr-old stems. In fact, Aleaf was
similar in S45, S52 and S80 with values of 213 38, 232 56
and 275 66 cm2, respectively. Significantly lower Aleaf was
recorded in S90 (93 16 cm2).
Figure 7 shows vulnerability curves for trees growing at the
four sites, as measured in the laboratory (black circles); the PLC
measured in the field throughout the season is also plotted vs the
corresponding Ψxyl measured in situ (open circles). Field-measured PLC values were well within the range of laboratory measurements. At all sites, VCs had a sigmoidal shape, and from the
regression curves the values of Ψxyl inducing 50% loss of hydraulic conductance (Ψ50) were calculated. These were lower in S45
and S52 ( 1.61 and 1.54 MPa, respectively), than in S80 and
S90 ( 1.37 and 1.28 MPa, respectively). In order to test the
statistical significance of site-specific differences in terms of vulnerability to cavitation, the average PLC induced by Ψxyl values
between 1.2 and 1.7 MPa was calculated (Fig. 8). Although
mean Ψxyl calculated in this range was not statistically different
across sites, PLC was found to be significantly higher in samples
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100
80
June
July
August
September
c
c
c
PLC (%)
bc
b
60
b
ab
b
40
a
a
a a
a
a
a
a
20
0
Miramare
S45
Scala
S52
Roiano
S80
Barcola
S90
(b) 0.0007
LSC (kg s–1 MPa–1 m–1)
0.0006
Native (ns)
Maximum (P < 0.05)
b
0.0005
0.0004
a
a
a
0.0003
0.0002
0.0001
0.0000
Miramare
S45
Scala
S52
Roiano
S80
Barcola
S90
Fig. 6 (a) Seasonal changes of percentage loss of hydraulic conductivity
(PLC) as measured in 2-yr-old stems sampled from Quercus ilex L. trees
growing at four experimental sites with different percentages of soil
surface pervious or impervious pavement cover (see Fig. 1). Mean values
are reported SD. (b) Leaf specific stem hydraulic conductivity (LSC) as
measured in 2-yr-old stems sampled in August 2013. Both native values
(black columns) and maximum values (gray columns) measured after
complete embolism removal are reported. Mean values are reported SD.
Different letters indicate statistically significant differences (P < 0.05).
ns, not significant.
from S80 and S90 than in those from S45 and S52. On the basis of
Ψ50 and minimum seasonal Ψxyl values, the safety margin toward
massive cavitation was calculated for trees growing at the different
sites (Choat et al., 2012). This was found to be slightly positive
in S45 and S52 (+0.01 and +0.04 MPa, respectively), but negative
in S80 ( 0.43 MPa) and S90 ( 0.72 MPa).
Across sites, VPD was not significantly correlated with the percentage of impermeable surface (P = 0.15). Also, no significant
correlation was observed between gL and VPD when single measurement periods or the whole dataset were considered, with the
exception of a significant inverse relationship observed in July
(r = 0.97, P = 0.03). By contrast, gL was inversely correlated to
the percentage of impervious pavement in June, August and September (P = 0.02–0.03), but not in July. PLC was not correlated
to VPD across sites, nor within each site on a seasonal basis. By
contrast, significant correlations between the amount of xylem
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embolism and the percentage of impervious pavement were
observed across sites in August (r = 0.94, P = 0.05) and September (r = 0.96, P = 0.04). In September Ψpd was found to decrease
with increasing percentage of impervious surface (Fig. 9a). However, PLC showed a positive correlation with the impermeability
level (Fig. 9b). Vulnerability to cavitation was positively correlated with the percentage of impervious surface, as progressively
less negative Ψ50 values were recorded at increasing percentage of
impermeable pavement (Fig. 9c). Finally, safety margins were
found to linearly decrease as a function of the impermeability
level across sites (Fig. 9d).
Discussion
A comparison of the water relations and hydraulics of holm oak
trees growing in four urban sites revealed clear patterns of increasing water stress exposure and vulnerability to drought at increasing percentages of impermeable soil coverage. The consequent
reduction in stomatal aperture, increase of embolism and vulnerability to cavitation, are all factors portending potential risks of
dieback under future climate scenarios for trees growing in urban
areas.
Plants growing in urban sites with largely paved surfaces experienced significantly higher levels of water stress than those growing in largely unpaved urban sites. Plant water status measured in
early summer, following abundant and prolonged rainfall, was
overall similar across sites. However, large differences were
recorded in August, when Ψpd, Ψmin and Ψxyl were more negative in sites with higher percentages of impervious surface (Figs 4,
9a). These differences might have been caused by higher evaporative demand (Chen et al., 2011; Pataki et al., 2011) and/or by
reduced water supply. Indeed, VPD was higher at the extensively
paved sites, but gL was apparently not strictly related to this
parameter (see the Results section). Impermeable surfaces have
been reported to prevent or delay rainfall infiltration in the soil
(Morgenroth et al., 2013), reducing the amount of water available to plants. Restricted water availability in paved sites would
be confirmed by recorded differences in terms of Ψpd, that is
assumed to reflect soil water potential as far as nocturnal transpiration is low (Kavanagh et al., 2007). In particular, the lack of
recovery of plant water potential following late-summer rains in
the extensively paved sites (Fig. 4) supports the existence of water
supply limitations. Moreover, impervious surfaces may limit not
only water penetration in the soil, but also soil–atmosphere gas
exchange, thus creating conditions restricting root growth (Day
et al., 2010; Viswanathan et al., 2011) and metabolism with
impacts on root hydraulics (Nardini et al., 1998).
The water potential drop during the summer drought translated into a decrease of gL at the study sites, but this was larger at
extensively paved sites. Moreover, at these sites stomatal aperture
was not restored following late summer rains, despite the large
decrease in VPD, whereas at the other sites gL returned to prestress values (Fig. 3). As a consequence, the time interval available
for net photosynthesis and carbon gain was significantly shortened at those sites with impermeable surfaces. Fluorescence
analysis suggested the occurrence of drought-induced
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100
90
80
Miramare, S45
Scala, S52
Ψ50 = –1.61 MPa
Ψ50 = –1.54 MPa
70
60
50
40
30
20
PLC (%)
10
0
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
100
90
80
Roiano, S80
Barcola, S90
Ψ50 = –1.37 MPa
Ψ50 = –1.28 MPa
70
60
50
40
30
20
10
0
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
−Ψxyl (MPa)
80
Ψxyl = –1.54 (SD = 0.18)
Ψxyl = –1.59 (SD = 0.19)
20
Ψxyl = –1.51 (SD = 0.17)
40
Ψxyl = –1.55 (SD = 0.18)
PLC (%)
60
Miramare
S45
Scala
S52
Roiano
S80
Barcola
S90
0
Fig. 8 Percentage loss of hydraulic conductivity (PLC) of 2-yr-old stems, as
measured at a mean xylem water potential (Ψxyl) of 1.5 MPa. Stems
were sampled from Quercus ilex trees growing at four experimental sites
with different percentages of soil surface pervious or impervious pavement
cover (see Fig. 1). Means are reported SD. Values recorded in Roiano
and Barcola are significantly higher than those of Miramare and Scala
(P < 0.05).
impairment of PSII in trees growing at sites with largely impermeable surfaces, indicating that these plants also suffered nonstomatal limitations of photosynthesis (Flexas et al., 2014).
Because photosynthesis limitations lead to progressive depletion
of nonstructural carbohydrates (Sevanto et al., 2014), urban trees
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Fig. 7 Vulnerability curves reporting the
relationship between percentage loss of
hydraulic conductivity (PLC) of 2-yr-old
stems, as measured at progressively lower
xylem water potential (Ψxyl). Stems were
sampled from Quercus ilex trees growing at
four experimental sites with different
percentages of soil surface pervious or
impervious pavement cover (see Fig. 1).
Closed circles, experimental points measured
in the laboratory during bench-dehydration
of branches sampled in the field; open circles,
mean values ( SD) recorded in the field
from June to September (see also Figs 4, 6).
The sigmoidal regression is reported together
with the calculated Ψxyl value inducing 50%
loss of hydraulic conductivity (Ψ50).
exposed to chronic water stress might also become more susceptible to other abiotic or biotic stress factors (Galvez et al., 2013;
Gaylord et al., 2013; Meineke et al., 2013).
Xylem water is subjected to negative pressure, and hence it is
prone to cavitation, but the likelihood of massive xylem cavitation and embolism increases at progressively decreasing Ψxyl values, according to species-specific vulnerabilities (Choat et al.,
2012). Xylem cavitation and embolism result in a reduction of
plant hydraulic conductance, which reduces gas exchange rates
and photosynthetic productivity, and also exposes plants to the
risk of hydraulic failure and desiccation (Trifilo et al., 2014b). In
the present study, the lower Ψxyl of trees growing at sites with
highly impermeable surfaces translated into higher stem PLC,
especially in August and September. At the peak of summer
drought (Figs 6, 9b), PLC reached values as high as 70%, close to
the limit that has been reported to be critical for woody angiosperms (Nardini et al., 2013). Moreover, at the site with the highest percentage of impervious surface, PLC did not recover even
after late-summer rains, suggesting that plants growing in urban
sites with paved soils experience a long-lasting risk of hydraulic
failure.
Previous studies have reported acclimation of vulnerability to
cavitation of some tree species, with Ψ50 values shifting toward
lower values in response to moderate water stress (Beikircher &
Mayr, 2009; Awad et al., 2010; Wortemann et al., 2011). In the
present study, however, vulnerability analysis revealed that individuals exposed to more intense water stress were more, and not
less, vulnerable to drought-induced cavitation, as revealed by
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Research 1113
(a)
–0.5
Miramare
r 2 = 0.88
P < 0.05
Scala
(b)
90
–0.6
Barcola
70
Roiano
–0.7
PLC (%)
Ψpd (MPa)
r 2 = 0.93
P < 0.05
80
–0.8
60
50
Roiano
40
Scala
–0.9
30
Barcola
–1.0
20
–1.1
70
80
90
100
50
60
70
80
0.2
Barcola
–1.4
Scala
–1.6
90
100
r 2 = 0.96
P < 0.05
Scala
Roiano
–1.5
40
(d)
r 2 = 0.99
P < 0.05
0.0
Miramare
–0.2
–0.4
Roiano
–0.6
Miramare
Barcola
–1.7
–0.8
40
50
higher Ψ50 values at extensively paved sites than at more natural
ones (Figs 7, 9c). Similar trends have been previously reported
for plants exposed to chronic or extreme water stress, and have
been interpreted as evidence of a ‘cavitation fatigue’ phenomenon
(Hacke et al., 2001) that would progressively increase vulnerability to cavitation, thus leading to hydraulic deterioration of the
xylem system (Anderegg et al., 2013; Nardini et al., 2014). The
lowest Ψ50 value recorded in the present study was 1.6 MPa
(Fig. 7), and even in the case of VC elaboration by subtracting
the PLC values recorded from fully rehydrated samples (c. 20%),
Ψ50 would still remain c. 2.3 MPa. These values are in accordance with Ψ50 values reported in the literature for holm oak by
Tognetti et al. (1998), but higher than more recent estimates for
the species (e.g. 3.2 MPa; Pinto et al., 2012). Although we cannot rule out that these differences are driven by genotypic plasticity, it has to be noted that Ψ50 variability across populations of
woody plants has been suggested to be narrow in the few species
tested (Wortemann et al., 2011; Lamy et al., 2014). On this basis,
we suggest that the higher vulnerability to cavitation of urban
holm oak trees subjected to the most intense and long-lasting
water stress might be interpreted as evidence for hydraulic deterioration caused by cavitation fatigue. Indeed, the fact that some
other studies focused on natural populations of holm oak found
significantly more negative Ψ50 values than those reported here,
would be in accordance with a ‘hydraulic degradation’ scenario
for our study trees. Our data would also be in accordance with a
study by Limousin et al. (2010) that reported increased vulnerability to cavitation in holm oak trees subjected to a 6-yr partial
rainfall exclusion.
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New Phytologist Ó 2014 New Phytologist Trust
60
–1.3
Ψ50 (MPa)
Fig. 9 Correlations between percentages of
soil surface covered by impervious pavement
and (a) predawn leaf water potential (Ψpd),
(b) percentage loss of hydraulic conductivity
(PLC), (c) xylem water potential inducing
50% PLC (Ψ50) and (d) safety margin
calculated as the difference between Ψ50 and
minimum seasonal xylem water potential
(Ψxyl), as measured in Quercus ilex trees
growing at four experimental sites (see
Fig. 1). Mean values are reported ( SD). The
regression lines together with r2 and P values
are also reported.
50
Safety margin (MPa)
40
(c) –1.2
Miramare
10
60
70
80
90
100
40
50
60
70
80
90
100
Impervious surface (%)
As a consequence of lower seasonal Ψxyl and intrinsically
higher Ψ50, the safety margin toward hydraulic failure (Choat
et al., 2012) was negative at those sites with large impervious surfaces, whereas it was slightly positive at the more natural sites
(Fig. 9d). Although the physiological significance of the safety
margin calculated over Ψ50 can be questioned, our findings do
reveal that urban trees can easily surpass critical xylem water
potential thresholds. This behavior might increase the risks of
canopy dieback upon increased exposure to extreme drought and
heatwaves (Helama et al., 2012), and might indeed represent an
important factor underlying the reported spatial patterns of tree
mortality in urban areas, with higher die-off rates observed in
areas with high soil compaction and/or impermeabilization (Nowak et al., 2004). Our data suggest that appropriate design of
urban green spaces, with special care given to limiting impermeable sealing of natural soil, might contribute to reduce the risk of
tree decline, thus improving the effectiveness of mitigation strategies based on street tree planting.
Despite significantly different PLC levels recorded in August,
native LSC was not different across sites, whereas LSC measured
after embolism removal was higher in the most water-stressed
trees (S90), in accordance with similar data reported for holm oak
by Limousin et al. (2010). This pattern was not due to compensatory changes in xylem anatomy, as vessel dimension and densities
were not significantly different across sites. Maintenance of
invariant LSC at increasing PLC was apparently achieved by
reducing the leaf surface area supplied by stem xylem. Previous
studies have also suggested that morphological adjustment is a
key mechanism adopted by plants to match invariant or increased
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1114 Research
transpiration demand with reduced soil water availability
(Limousin et al., 2010; Vaz et al., 2012), and urban trees make
no exception in this sense. From a practical point of view,
adjustment of leaf area with increasing PLC might imply a reduction of canopy leaf surface area and, hence, a decrease in the shading provided by urban trees, which is key to the cooling effect of
urban vegetation (Armson et al., 2012). Hence, even though
morphological adjustment through changes in biomass allocation
might help urban trees to cope with drought, the urban ecological value of trees growing in the most stressful sites is likely to
be reduced via hydraulic effects related to vulnerability to
cavitation.
In conclusion, our data revealed new correlations between soil
conditions, plant water status and hydraulic vulnerability of trees
growing in urban areas. Growth conditions, with special reference to the amount of impermeable surface surrounding trees,
influenced site-specific water status and drought vulnerability.
However, data must be interpreted with caution, as several other
confounding variables that might affect the physiology of urban
trees were not explicitly investigated in this study. The study provides practical information for tree management in urban sites,
but also suggests that key plant processes and responses such as
drought-induced xylem cavitation, hydraulic deterioration and
hydraulic adjustment are fundamental for a full understanding of
responses of urban trees to environmental stresses. The study of
urban tree hydraulics holds important promise in developing better adaptation strategies addressed at improving the sustainability
of urban areas under ongoing climate changes.
Acknowledgements
The study was funded by MIUR (Ministero dell’Istruzione,
dell’Universita e della Ricerca) under the project PRIN 2010–
2011 TreeCity (Progettare la citta verde nell’era del cambiamento
globale: funzioni degli alberi urbani e loro adattabilita nelle
future condizioni climatiche) and by University of Trieste (Finanziamento di Ateneo per la Ricerca Scientifica 2013 – Cambiamenti climatici e mortalita delle foreste: dai meccanismi
fisiologici alle conseguenze ecologiche). The study is also linked
to activities conducted by A.N. within the COST Action FP1106
STReESS (Studying tree responses to extreme events: a synthesis). We are grateful to the local municipality (Comune di Trieste, Servizio Verde Pubblico) for allowing us to collect samples
from experimental trees. We are also grateful to M. Marin and
D. Boldrin for technical assistance during field measurements.
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