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TreesStructure and Function ISSN 0931-1890Volume 27Number 6 Trees (2013) 27:1691-1701DOI 10.1007/s00468-013-0916-7
Hydraulic properties of European elms:xylem safety-efficiency tradeoff and speciesdistribution in the Iberian Peninsula
Martin Venturas, Rosana López,Antonio Gascó & Luis Gil
1 23
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ORIGINAL PAPER
Hydraulic properties of European elms: xylem safety-efficiencytradeoff and species distribution in the Iberian Peninsula
Martin Venturas • Rosana Lopez • Antonio Gasco •
Luis Gil
Received: 25 March 2013 / Revised: 18 July 2013 / Accepted: 26 July 2013 / Published online: 14 August 2013
� Springer-Verlag Berlin Heidelberg 2013
Abstract
Key message Ulmus minor and U. glabra show a trade-
off between safety and efficiency in water transport, and
U. laevis shows adaptations to waterlogged environments.
Abstract Three native elm species grow in Europe: Ulmus
minor Mill., U. glabra Huds. and U. laevis Pall., and within
the Iberian Peninsula their habitats mainly differ in water
availability. We evaluated firstly whether vulnerability to
xylem embolism caused by water-stress has been a deter-
minant factor affecting their distribution; secondly, if their
xylem anatomy differs due to water availability dissimi-
larities; and thirdly, if these species present a trade-off
between water transport safety and efficiency. Plants of the
three species were grown in a common-garden in Madrid,
Central Spain. The centrifuge method was used for con-
structing the vulnerability curves, and anatomical mea-
surements were carried out with an optical microscope. We
found clear differences in conductivity and cavitation
vulnerability between the three species. Although all three
elms were highly vulnerable to cavitation, U. minor was
significantly more resistant to water stress cavitation. This
species reached 50 % loss in conductivity at -1.1 MPa,
compared to U. glabra that did so at -0.5 MPa, and U.
laevis at -0.4 MPa. Maximum xylem specific conductivity
and maximum leaf specific conductivity were two to three
times higher in U. glabra when compared to U. minor. A
clear trade-off between safety against losses of conduc-
tivity and water transport efficiency was observed consid-
ering both U. minor and U. glabra samples. Ulmus minor’s
hydraulic configuration was better adapted to overcome
drought episodes. The expected aridification of the Iberian
Peninsula could compromise Ulmus populations due to
their high vulnerability to drought stress.
Keywords Drought tolerance � Elm species
distribution � Ulmus � Waterlogging stress �Wood anatomy � Xylem cavitation
Introduction
Three elm species grow naturally in Europe: Ulmus minor
Mill. (Field elm), U. glabra Huds. (Wych elm), and U. laevis
Pall. (White elm) (Richens 1983). The first two are closely
related, hybridise easily (Mittempergher and La Porta 1991),
and belong to section Ulmus (Wiegrefe et al. 1994); whereas
U. laevis is incompatible with the other two species (Mit-
tempergher and La Porta 1991) and belongs to section
Blepharocarpus (Wiegrefe et al. 1994). These three elms
inhabit different environments and niches within the Iberian
Peninsula (Figs. 1, 2). Ulmus minor is adapted to warmer
climates (Collin et al. 2000), and can tolerate moderate
summer drought. It inhabits lowland floodplain forests
(0–1,650 m). Its roots tap the groundwater-table (Fig. 2).
Communicated by Y. Sano.
M. Venturas � R. Lopez � L. Gil (&)
GENFOR Grupo de Investigacion en Genetica y Fisiologıa
Forestal, Departamento de Silvopascicultura, E.T.S.I. Montes,
Universidad Politecnica de Madrid, Ciudad Universitaria S/N,
28040 Madrid, Spain
e-mail: luis.gil@upm.es
M. Venturas
e-mail: martin.venturas@upm.es
R. Lopez
e-mail: rosana.lopez@upm.es
A. Gasco
IE University, Cardenal Zuniga 12, 40003 Segovia, Spain
e-mail: amgasco@faculty.ie.edu
123
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DOI 10.1007/s00468-013-0916-7
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Ulmus glabra grows in the North within Euro-Siberian for-
ests, and in the Eastern and Central mountains. It is found
either close to streams, or in cool valleys of water-table
discharge areas (Rossignoli and Genova 2003). It suffers a
dry season shorter than 1 month (0–1,800 m, Fig. 1). Ulmus
laevis populations are either riparian, or related to seasonally
waterlogged soils of aquifer discharge areas or small closed
basins (0–1,650 m; Figs. 1, 2; Venturas et al. 2013a). This
species can tolerate prolonged flooding (Collin 2003).
In Spain, it is estimated that more than 60 % of wetlands
have disappeared during the last 50 years due to anthro-
pogenic landscape changes (Gallego-Fernandez et al.
1999). The expected climate change scenario for the Ibe-
rian Peninsula forecasts longer and more intense drought
periods (Somot et al. 2008; De Luis et al. 2010). This will
probably increase water demand for irrigation, which
ultimately may cause further depletion of current water
tables level, thus significantly affecting the configuration
and conservation of riparian forests.
An important physiological consequence related to this
forecast is that more frequent hydraulic failure episodes are
expected to occur within xylem vessels under higher water
stressing environments. This results in the disruption of the
soil–plant-atmosphere continuum and a consequent higher
reduction in water supply to the leaves (Sperry and Tyree
1988). In fact, xylem vulnerability to drought-induced
cavitation has been addressed as one of the major factors
affecting plant productivity and survival (Tyree and Sperry
1988; Sperry et al. 2008; Lopez et al. 2013), and conse-
quently it has been considered an explanation for the
environmental distribution of many species (e.g. Nardini
et al. 2010; Rood et al. 2003; Maherali et al. 2004; Tissier
et al. 2004; Jacobsen et al. 2008; Aref et al. 2013).
Water availability exerts a strong control over xylem
anatomy. As a result, the structure of xylem conduits
markedly differs among populations of the same species
growing under contrasting environmental conditions
(Carlquist 1977). Plant hydraulic architecture is the result
Fig. 1 Distribution of the three native elm species in Spain and
populations from which seeds were collected with their Walter–Leith
climodiagrams. Above the climograph panels, from left to right:
population altitude, mean annual temperature and mean annual
precipitation. To the left of the temperature axis, from top to bottom:
mean annual maximum temperature, mean of the daily maximum
temperatures of the warmest month, mean of the daily minimum
temperatures of the coldest month, and mean annual minimum
temperature. Black rectangles under the months indicate frost period;
vertical bar shading indicates humid period; dotted shading indicates
drought period. Climatic data belongs to the records collected from the
following weather stations (MAGRAMA, 2012): ‘Segovia Observato-
rio’ [1,005 m, 408570N, 4�70W, 43 year record (1961–2003) for
precipitation (P) and temperature (T)], ‘Presa de Burguillo’ [750 m,
408250N, 4�310W, 38 (1961–1999) and 25 (1974–1999) year records for
P and T, respectively], and ‘Madrid Puerta de Hierro’ [630 m, 408270N,
38440W, 20 year record (1961–1988) for P and T]. Climatic data was
corrected for altitude (-0.65 �C and ?8 % precipitation changes per
100 m height increase). The distribution map was elaborated using the
following data sources: Ulmus glabra Huds. (Rossignoli and Genova
2003), U. minor Mill. (Garcıa-Nieto et al. 2000), and U. laevis Pall.
(Venturas et al. 2013a)
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of a trade-off between water transport efficiency from roots
to leaves, and safety against runaway embolism through the
xylem (Sperry 2003). Environmentally-induced differences
in vessel sizes explain changes in plant hydraulic conduc-
tance (e.g. Pammenter and Van der Willigen 1998).
Globally there is no connection among vessel length and
width, and only the latter is strongly influenced by envi-
ronment (Jacobsen et al. 2012). Wider and longer vessels
are more efficient transporting water (according to the
Hagen–Poiseuille law), but they are also expected to be
less safe against cavitation occurrence within a plant
(Tyree and Zimmerman 2002). Wider conduits are also
more susceptible to freezing-induced embolism (Davis
et al. 1999; Pittermann and Sperry 2003). Vessel length
was identified as the central parameter explaining differ-
ences in the specific hydraulic conductivity of seven Acer
species, emerging as a critical trait of the safety-efficiency
trade-off within this genus (Lens et al. 2011).
Intervessel pitting is also considered to play a determining
role in this empirical trade-off. Differential pit membrane
pore sizes and distributions have been correlated to inter- and
intraspecific differences in xylem vulnerability to cavitation
and xylem water transport efficiency (Jarbeau et al. 1995;
Vander Willigen et al. 2000; Christman et al. 2009; Jansen
et al. 2009). The ‘pit area hypothesis’ (Wheeler et al. 2005)
and the ‘rare pit hypothesis’ (Christman et al. 2009), both
propose that a species with larger and longer conduits tend to
have a greater pitted wall area; which, in turn, may lead to a
greater probability of having large pit membrane pores that
are more vulnerable to air seeding. Those plants showing a
greater redundancy within their vascular pathway (i.e. many
small vessels) are expected to be intrinsically safer against
embolism-induced losses of conductivity than those that rely
on a small number of large very efficient vessels for water
transport (Sperry and Tyree 1988; Sperry et al. 2008).
Since climate and groundwater availability are the main
differences between the niches of these elm species, our
predictions are: (i) that U. minor has a higher resistance to
drought-induced xylem cavitation than U. laevis and U.
glabra, as it is able to overcome certain summer drought,
and this might explain elm species geographic distributions
within the Iberian Peninsula; (ii) that differences in water
availability in their natural habitats affect elm species’
xylem anatomy, which also determines their efficiency in
supplying water to the leaves; and (iii) that there is a trade-
off between xylem hydraulic conductance and cavitation
resistance among these elm species. A common garden
experiment was designed and carried out in order to verify
these predictions.
Materials and methods
Plant material
Ulmus minor seeds were sampled at Puerta de Hierro
nursery’s conservation plot (Madrid; 40�270N, 3�450W); U.
glabra samaras were gathered in Valle de Iruelas forest
(Avila; 40�210N, 4�360W); and U. laevis seeds were col-
lected in a wetland woodland located in Palazuelos de
Eresma (Segovia; 40�540N, 4�30W) (Fig. 1). All seeds were
collected during 2005–2007 and were preserved dry
(\10 % moisture) in a cold-storage chamber (4 �C) until
used.
Seeds were sown in March 2007, and seedlings were
then grown in 0.35 L forest-pot containers at Puerta de
Hierro nursery under partial shading (60 %). The used
substrate was 25 % perlite and 75 % peat (v:v) enriched
with 2 g L-1 of slow release fertiliser [Osmocote� Plus
Standard, 15:9:12 (N:P:K); 12–14 month release]. One
U. laevis
U. minor
U. glabra Silicious soils
Calcareous soils
Groundwater table
Water
Endorheic basins &seasonal wetlands
River & floodplains
Mountains & shadygullies
Maximum flood level
Fig. 2 Habitat sketch for the three European elms in Spain
Trees (2013) 27:1691–1701 1693
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year later, they were transplanted to 3 L forest-pot con-
tainers filled with the same substrate mixture. Plants were
always grown under well-watered conditions.
Finally, seedlings were transplanted to a well-watered
experimental plot located within the same nursery follow-
ing a 0.55 9 1.00 m spacing sketch in March 2010. 476
plants, belonging to 15 U. minor, 9 U. glabra, and 12 U.
laevis families, were planted. They were grouped in
experimental units made up of four plants of the same
family which were randomly distributed in two complete
unbalanced blocks. The plot was surrounded by a border
line of elms which were not selected for any measure-
ments. Elms were 2.3 ± 0.4 m tall (mean ± standard
deviation) when measurements were carried out in August
2011. Five families of each of the 3 elm species and 2 trees
per family (i.e. 30 trees in total, 10 per species) were
randomly selected to perform the measurements described
next.
Vulnerability curves and xylem hydraulic conductivity
Xylem vulnerability curves (VC) were determined for the
selected trees during the last week of August, 2011. One
south-orientated branch from the top half of every ran-
domly selected tree was collected for this purpose. These
branches were 1-year-old and 2–4 mm in diameter. Each
sampled branch was cut under water and immediately
transported to the laboratory, where a 14 cm-long section
was re-cut under water just before determining its VC.
The hydraulic conductivity (K, kg m s-1 MPa-1; Sperry
et al. 1988) of these stem segments was measured using a
XYL’EM device (Xylem Embolism Meter, Bronkhorst,
Montigny les Cormeilles, France) at low pressure
(2–3 9 10-3 MPa), perfusing the samples with filtered
(0.2 lm) degassed 10 mM KCl and 1 mM CaCl2 solution
(Herbette and Cochard 2010). Native conductivity (KN)
was immediately measured after cutting stem samples
under water. Next, their native embolism was removed by
applying high-pressure flushing (0.16 MPa) for 30 min;
and their maximum hydraulic conductivity (Kmax) was then
measured. Native percentage loss of conductivity (PLCN)
was then calculated as PLCN = 100(Kmax - KN)/Kmax.
VCs were built applying the centrifugal-force methodol-
ogy, as described in Alder et al. (1997), using a 15 cm rotor
that fits three 14 cm-long samples at a time. After deter-
mining their Kmax, stem samples were subjected to
increasing pre-set pressure steps (-0.25, -0.5, -1.0, -1.5,
-2.0, -3.0 and -4.0 MPa) that were held in the centrifuge
for 6 min. Kh was measured in the XYL’EM after
imposing and relaxing each pressure level, and the result-
ing percentage loss of conductivity [PLC = 100�(Kmax -
Kh)/Kmax] induced in each stem segment was determined.
A minimum 85 PLC was achieved in all the samples after
applying -4.0 MPa. All measurements were performed in
a laboratory at 20 �C.
Each VC was fitted to an exponential sigmoid
[PLC = 100/(1 ? exp(a�(W - b))); Pammenter and Van
der Willigen 1998] using SigmaPlot 10.0 software (Systat
Software, Inc.). Applied pressures (MPa) at which 50 PLC
(P50, b parameter of the fitted sigmoid) and 80 PLC (P80)
were reached were obtained from the fitted model equa-
tions. Maximum xylem-specific conductivity (KS,
kg m-1 s-1 MPa-1) was calculated by dividing Kmax by
each sample’s xylem cross-sectional area (AS, m2; e.g.
Hultine et al. 2006).
Specific leaf area and leaf-specific xylem hydraulic
conductivity
All leaves distal to the stem section used for determining its
VC were collected, counted (NL), and scanned (Epson
Expression 10000 XL scanner) in order to determine the
total leaf area (AL, cm2) with WinFOLIA software (Regent
Instruments Inc., Canada). All collected leaves were then
oven-dried at 75 �C for 48 h, and leaf dry mass (ML, g) was
also measured. Specific leaf area (SLA, cm2 g-1) was
calculated as the ratio AL:ML.
Dry season native leaf-specific xylem conductivity
(KL-N, kg m-1 s-1 MPa-1) was calculated dividing KN by
AL (Jacobsen et al. 2008). The ratio between the leaf area
that is sustained by each unit of xylem area was also
determined (AL:AS).
Wood density
2.5 cm-long segments were cut from the left over basal part
of the branches selected for VC determination in order to
determine its wood density (WD, g cm-3), using the same
methodology described in Hacke et al. (2000). These stem
segments were longitudinally split, and bark and pith were
easily removed using a razor blade. The resultant xylem
segments were soaked in degassed water overnight; and
their saturated wood volume was then determined,
according to Archimedes’ law, immersing each sample in a
water-filled test tube placed on a balance. Displacement
water weight was converted to sample volume considering
water density (0.9982071 g cm-3 at 20 �C). Wood samples
were then stored at 75 �C for 48 h, after which their dry
weight was measured. WD was calculated as the ratio of
dry weight to saturated volume.
Xylem anatomical traits
Five stem segments per elm species (one per family) of
those used for building up VCs were randomly selected to
perform anatomical measurements. 2 cm-long transverse
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wood disks were sampled at the basal end of each stem
segment, and were placed in a formaldehyde-acetic acid-
70 % ethanol fixative (5:5:90, v:v:v). 15 lm-thick trans-
verse sections were cut using a sliding microtome (Leica
SM 2400), were then stained with safranin 0.1 % (weight/
volume), dehydrated through an ethanol series, mounted on
microscope slides, and fixed with Canada balsam for light
microscopy observation.
Images of the prepared transverse cuts were taken using
a camera (5 MPx) attached to an Olympus BX50 light
microscope. Measurement of anatomical features was
performed using WinCELL image analysis software
(Regent Instruments Inc., Canada). Four randomly-selected
458 circular sectors were analysed per sample, in which
vessel frequency (VF, vessels mm-2), vessel area (VA,
lm2), and vessel lumen transectional area in relation to
total xylem area (VTA, %; Lovisolo and Schubert 1998)
were measured. Vessels with a smaller diameter than
20 lm were not considered for analyses. Vessel diameter
(VD, lm) was estimated from a circle of an equal VA; and
vessel diameter distributions were composed considering
10 lm width classes.
Hydraulic vessel diameter (Dh) was calculated in each
sector dividing the sum of vessel diameters to the fifth power
by the sum of vessel diameters to the forth power
(Dh =P
VD5/P
VD4) (Kolb and Sperry 1999). The theo-
retical hydraulic conductance (THC, lm2) predicted by the
Hagen–Poiseuille equation (Giordano et al. 1978) was
determined dividing the sum of the fourth power of all
internal vessel radii found within each xylem sector by the
total area of that sector (ASector) (THC =P
(VD/2)4/ASector).
Moreover, the percentage of grouped vessels (PGV, %)
was estimated by counting all grouped and non-grouped
vessels considering three different xylem areas that were
identified within each sampled cross-section: wood adjacent
to the pith (PGVP), earlywood (PGVEW) and latewood
(PGVLW). Finally, the tangential lumen span (b), and the
thickness of the double wall (t) of all adjacent vessels within
them, were measured in four randomly-selected square
sectors (0.7 mm2) of earlywood; and inter-vessel wall
strength was calculated as (t/b)2 following Hacke et al.
(2001).
Data processing and statistical analyses
One-way analyses of variance (ANOVA) considering
species as the only factor were performed for maximum
hydraulic conductivity, and for the parameters of the VCs.
A nested ANOVA design, considering tree nested within
species, was used for anatomical measurements. All pair-
wise comparisons of mean values were performed using
Tukey’s (HSD) multiple range test at a 95 % confidence
level. Pearson’s product-moment correlation coefficient (r),
and its statistical significance (P value), were calculated in
order to assess relations between variables and possible
tradeoffs between xylem safety against cavitation and
water transport efficiency. All statistical analyses were
performed using STATISTICA 7.0 software (StatSoft Inc.,
Oklahoma, USA).
Results
Ulmus minor and U. laevis grew 30 cm taller and showed
wider diameter at breast height than U. glabra (Table 1).
Although U. minor developed more leaves per branch (NL)
than the other two species (Table 1), they were signifi-
cantly smaller. AL:AS was lower in U. minor than in U.
laevis. The latter showed the highest SLA (Table 1).
Ulmus minor branches showed the highest WD
(Table 1). Vessel frequency (VF) and the percentage of
grouped vessels in both latewood (PGVLW) and earlywood
(PGVEW) were significantly higher in U. laevis than in the
other two species. Average vessel lumen area (VA) ranged
from 941 ± 22 lm2 in U. minor to 1,392 ± 22 lm2 in U.
glabra (Table 2). The former species showed the highest
Table 1 Plant morphology and leaf characteristics of the elms used in this study (n = 10 per species)
Variable Units U. minor U. glabra U. laevis P value
H m 2.4 ± 0.1b 2.1 ± 0.1a 2.4 ± 0.1b 0.0068
D cm 1.5 ± 0.2b 0.9 ± 0.1a 1.3 ± 0.1ab 0.0287
NL 40.8 ± 6.8b 12.9 ± 1.2a 15.7 ± 0.6a 0.0000
SLA cm2 g-1 96.6 ± 4.4a 94.5 ± 2.4a 119.1 ± 4.7b 0.0002
AL:AS 4,091 ± 326a 5,376 ± 431ab 6,481 ± 520b 0.0024
WD g cm-3 0.84 ± 0.05b 0.62 ± 0.03a 0.71 ± 0.03a 0.0016
Mean values ± standard errors and P value for one-way ANOVAs
Letters label homogeneous groups within a variable (Tukey’s HSD method)
H plant height, D plant diameter at 1.3 m above the ground, NL number of leaves, SLA specific leaf area, AL:AS, leaf area divided by xylem area,
WD wood density
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proportion of small vessels, whereas the latter had the
highest proportion of large vessels and larger hydraulic
diameter (Dh) (Table 2; Figs. 3, 4). Vessel lumen trans-
actional area (VTA) and THC were the highest for U.
glabra, and the lowest for U. minor (Table 2); whereas
inter-vessel wall strength (t/b)2 was estimated to be sig-
nificantly lower in U. laevis (Table 2).
Hydraulic conductivity was clearly different among the
three elm species (P \ 0.01; Table 3). Ulmus glabra
showed 2–3 times higher KS and KL-N than the other two
elm species; and there were no significant statistical dif-
ferences between the conductivities of U. minor and U.
laevis (KS and KL-N). In addition, all these elm species did
not show significant differences in the PLCN (P = 0.49;
Table 3).
Despite xylem vulnerability to cavitation being high in
all elms, U. minor was significantly less vulnerable than the
other two species (Table 3; Fig. 5). Pressures at which 50
and 80 % loss of conductivity were reached (P50 and P80)
were respectively about -1 and -2 MPa for this species;
whereas U. glabra and U. laevis showed approximately
half these values. Ulmus laevis’ vulnerability slope was
significantly the steepest (Table 3; Fig. 5). Ulmus glabra
and U. laevis had similar VCs in relation to PLC (Fig. 5a),
but U. glabra maintains higher hydraulic conductivities
(KS) with declining water potentials (Fig. 5b).
Table 2 Xylem anatomic features of the three European elm species (n = 5 per species)
Variable Units U. minor U. glabra U. laevis P value
VF vessels mm-2 60.8 ± 4.2a 71.4 ± 2.4b 80.7 ± 4.8c 0.0000
VA lm2 941 ± 22a 1,392 ± 22c 1,048 ± 23b 0.0000
VTA % 5.9 ± 0.4a 10.0 ± 0.3c 9.0 ± 0.4b 0.0000
Dh lm 43.4 ± 1.7a 56.6 ± 1.0b 48.6 ± 2.4a 0.0000
THC lm2 7.2 ± 0.8a 20.1 ± 1.1c 10.3 ± 0.7b 0.0000
(t/b)2 0.051 ± 0.003b 0.058 ± 0.006b 0.040 ± 0.003a 0.0009
PGVP % 98.5 ± 2.5a 91.7 ± 2.3a 99.5 ± 2.1a 0.0559
PGVEW % 48.3 ± 3.4a 45.8 ± 3.3a 73.9 ± 3.2b 0.0000
PGVLW % 87.8 ± 2.5a 88.4 ± 2.2a 96.7 ± 1.5b 0.0093
Mean values ± standard errors and P value for one-way ANOVAs
Letters label homogeneous groups within a variable (Tukey’s HSD method)
VF vessel frequency, VA average vessel area, VTA vessels lumen transectional area, Dh hydraulic diameter, THC theoretical hydraulic con-
ductance, (t/b)2 inter-vessel wall strength, PGVP percentage of grouped vessels in wood adjacent to the pith, PGVEW percentage of grouped
vessels in earlywood, PGVLW percentage of grouped vessels in latewood
Fig. 3 Cross-sectional xylem images: U. minor (a, d), U. glabra (b, e), and U. laevis (c, f). Scale bars correspond to 500 lm in a, b and
c images, and to 200 lm in d, e and f
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Parameters of the VCs, P50 and P80, were not well
correlated with KS (n = 29, P [ 0.05; one U. minor VC
was an outlier, so it was not considered within analyses),
nor with WD (n = 29, P [ 0.05), when all three species
were considered; but they were when U. laevis data was
excluded from analyses; that is, when only U. minor and U.
glabra results were included in the plot (n = 19, P \ 0.05;
Fig. 6). P80 was positively correlated to SLA (n = 29,
R2 = 0.27, P \ 0.01; Fig. 6). On the other hand, PLCN
showed positive correlation with P50 (n = 30, R2 = 0.26,
P \ 0.01) and P80 (n = 29, R2 = 0.30, P \ 0.01; Fig. 6);
and WD was negatively correlated with KS (n = 30,
R2 = 0.15, P \ 0.05; Fig. 6). Finally, VTA and AL were
also positively correlated (n = 15, P \ 0.05; Fig. 6).
Discussion
Anatomical and hydraulic properties of three European elm
species were assessed following the growing of plants from
seeds under equal optimal growing environmental condi-
tions, so the inter-specific differences addressed here
should mainly be attributed to genotypic expression.
Our results show that these three elm species are, in
general, highly susceptible to drought-induced cavitation,
which has been previously reported for other riparian
species (e.g. Tyree et al. 1994; Hacke and Sauter 1995;
Swift et al. 2008) and for U. minor (Venturas et al. 2013b).
Vulnerability to cavitation of U. laevis, the most suscep-
tible species in our study, was in accordance to those
values previously reported for U. alata Michx., an endemic
species of the woodlands of South Eastern United States
(Domec et al. 2010), using the same centrifuge method to
determine the VCs. This method has been well reported to
produce comparable results to the air-injection or the bench
dehydration methods when a low pressure head is used to
measure conductivity (Sperry et al. 2012; Tobin et al.
2012).
Despite U. minor showing significantly lower vulnera-
bility (Table 3; Fig. 5), the high vulnerability to drought
stress cavitation shown by all these elm species may
indicate that they complementarily rely on other alterna-
tives for overcoming moderate water-stress. Possible
alternatives are stomatal closure or other mechanisms
reducing transpiration and photosynthetic rate (Hacke and
Sauter 1995; Alder et al. 1997; Rood et al. 2003), or leaf-
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50
60
70
20-30 30-40 40-50 50-60 60-70 70-80 >80%
of
vess
els
Vessel diameter classes (µm)
U. glabra
U. laevis
U. minor
U. glabra %THC
U. laevis %THC
U. minor %THC
Fig. 4 Vessel diameter
distributions for each elm
species (bars represent standard
deviation; and letters label
homogenous groups of mean
values identified by Tukey’s
HSD test), and contribution of
each diametric class to
theoretical hydraulic
conductance (% THC)
Table 3 Hydraulic features of the three European elms (n = 10 per species)
Variable Units U. minor U. glabra U. laevis P value
KS kg m-1 s-1 MPa-1 1.26 ± 0.23a 2.64 ± 0.18b 1.03 ± 0.28a 0.0001
KL-N kg m-1 s-1 MPa-1 104 2.35 ± 0.48ab 3.91 ± 0.73b 1.21 ± 0.39a 0.0071
PLCN % 18.6 ± 7.3a 27.6 ± 7.3a 30.6 ± 7.3a 0.4868
a MPa-1 2.6 ± 0.5a 7.3 ± 2.8ab 17.3 ± 4.8b 0.0034*
P50 MPa -1.13 ± 0.11a -0.50 ± 0.07b -0.38 ± 0.09b 0.0078
P80 MPa -2.07 ± 0.57a -0.91 ± 0.16ab -0.64 ± 0.20b 0.0225
Mean values ± standard errors and P value for one-way ANOVAs
Letters label homogeneous groups within a variable (Tukey’s HSD method)
KS maximum xylem-specific conductivity, KL-N native leaf specific xylem conductivity, PLCN native percentage loss of conductivity, a slope of
the vulnerability curves, P50 pressure at which a 50 % loss of conductivity is produced, P80 pressure at which an 80 % loss of conductivity is
reached
* This parameter was log transformed to meet ANOVA’s assumptions
Trees (2013) 27:1691–1701 1697
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shedding due to hydraulic and cavitation segmentation
(Tyree et al. 1993; Tsuda and Tyree 1997). When com-
pared with other riparian plants subjected to declining
water tables, mechanisms of Ulmus drought tolerance
seemed to rely on greater plasticity in root allocation and
intrinsic water use efficiency (Perry et al. 2013).
Certain significant trade-off relationships between
xylem conductivity efficiency and drought induced cavi-
tation were found considering only results for U. minor and
U. glabra (Fig. 6). The increase in KS was associated with
a decrease in P50, a consequence of larger vessels and
lower WD (Tables 1, 2, 3; Fig. 6). The larger PLC of U.
glabra is partly compensated with higher KS at water
potentials between 0 and -1 MPa (Fig. 5). These two
closely related elm species have probably undergone an
ecologically-based divergent selection along a soil mois-
ture gradient. U. minor has better adapted to drier envi-
ronments, where it has to withstand moderate drought
episodes, and therefore it has developed a higher resistance
to drought-induced cavitation.
Ulmus glabra has better adapted to wet environments
where no drought periods occur, so higher water transport
efficiency structures have been selected (Tables 2, 3;
Fig. 4; Sperry et al. 2008). Both U. laevis and U. glabra
presented higher AL than U. minor, and water supply to the
leaves was compensated by a higher VTA (Fig. 6). The
lower SLA values shown in U. minor and U. glabra are
probably due to their higher water usage efficiency than U.
laevis (e.g. Rodrıguez-Calcerrada et al. 2011). The positive
PLC
0
20
40
60
80
100
U. minor
U. glabra
U. laevis
ψ (MPa)-4 -3 -2 -1 0
KS (
kg m
-1 s
-1 M
Pa
-1)
0.0
0.5
1.0
1.5
2.0
2.5
3.0
(a)
(b)
Fig. 5 Vulnerability curves of 1-year-old stem xylem samples of the
three native elm species growing within the Iberian Peninsula. The
curves are represented as a percentage loss of conductivity and
b actual specific hydraulic conductivity at different water potentials
(bars represent standard errors)
KS (Kg m-1s-1MPa-1)
0 1 2 3 4
P 80(M
Pa)
-2.5
-2.0
-1.5
-1.0
-0.5
0.0
P = 0.01R 2 = 0.33
WD (g cm-3)
0.4 0.6 0.8 1.0 1.2 1.4
P 80 (
MP
a)
-2.5
-2.0
-1.5
-1.0
-0.5
0.0P = 0.03R 2 = 0.25
SLA (cm2g-1)
70 90 110 130 150
P 80 (
MP
a)
-2.5
-2.0
-1.5
-1.0
-0.5
0.0
WD (g cm-3)
0.4 0.6 0.8 1.0 1.2 1.4
KS (
Kg
m-1
s-1M
Pa-1
)
0
1
2
3
4
VTA (%)3 5 7 9 11 13
AL(c
m2 )
0
200
400
600
800
1000P = 0.01R 2 = 0.39
PLCN
0 20 40 60 80
P 80(M
Pa)
-2.5
-2.0
-1.5
-1.0
-0.5
0.0
P = 0.00R 2 = 0.30
P = 0.00R 2 = 0.27
P = 0.04R 2 = 0.14
Fig. 6 Correlation scatter plots for Ulmus minor (squares), U. glabra
(dots), and U. laevis (triangles). Solid line regression calculated
considering all the three species. Broken line regression calculated
excluding U. laevis data. P value and R2 correspond to the plotted
regression lines
1698 Trees (2013) 27:1691–1701
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correlation between P80 and SLA could point out that
plants growing in high water availability habitats need
neither to be water use efficient, nor to develop a high
resistance to drought-stress cavitation.
This hydraulic behaviour is in accordance with the
general tendency previously observed in closely related
species (e.g. Tissier et al. 2004). Resistance to cavitation
increased at the cost of the reduction of KS mainly through
a decrease of specific pit conductivity (Domec et al. 2010).
Larger conduits are often associated with more flexible pit
membranes of lower resistance to air-seeding (Domec et al.
2008; Hacke and Jansen 2009). Therefore, larger vessels
provide U. glabra with higher hydraulic conductance
(Tables 2, 3; Fig. 4), but also with higher vulnerability to
cavitation due to this complex ratio between vessel size and
pit area (Hacke et al. 2006). A significant positive corre-
lation was also observed between WD and cavitation
resistance (as in Pratt et al. 2007) just considering the
results of these two elm species (e.g. WD and P80 in
Fig. 6); but they did not differ in their resistance to lumen
implosion (t/b)2, possibly because the pressure threshold
that is necessary to induce cavitation is lower than the level
required to cause the vessel to collapse.
This safety-efficiency trade-off is not detected when U.
laevis is included in the analysis. As this species is
genetically more distantly related to the other two (Wieg-
refe et al. 1994), its pit membrane configuration might also
be more different. It has probably also undergone different
speciation and selection processes in order to be better
adapted to high water availability environments and
flooding (Collin 2003). The mechanisms by which flood-
tolerant plants survive waterlogging are complex and
involve morphological, anatomical, and physiological
adaptations (Kozlowski 1997). Root anoxia is among the
main stresses caused by waterlogging. Therefore, the
development of adaptation mechanisms favouring oxygen
uptake by aerial tissues, and its transport across the plant
(such as the production of hypertrophied lenticels, aeren-
chyma tissue, and adventitious roots) is required to ensure
plant growth and survival (Kozlowski 1997; Pardos 2004).
It has also been suggested that cavitated and embolised
xylem conduits may play an important role in oxygen
storage and transport (Philipson and Coutts 1980; Raven
1996; Sorz and Hietz 2005), as the diffusion coefficient of
oxygen in air is four orders of magnitude higher than in
water. As U. laevis lives in waterlogged soils, it would be
interesting to investigate whether its higher vulnerability to
cavitation might favour root and stem oxygen supply.
A trial applying ethrel to U. americana L. plants in order
to simulate waterlogging effects reported a reduction in
vessel size, whereas VF and clustering increased, in com-
parison to non-treated plants features (Yamamoto et al.
1987). Considering these traits as adaptations to flooding, it
is worth noting that U. laevis, which is the European elm
with the highest waterlogging tolerance, exhibited the
highest VF, PGVEW and PGVLW of the three Iberian elm
species (Table 2); its plants also developed smaller vessels
than U. glabra ones (Table 2), which is also a high water-
demanding species not tolerating drought, all grown under
optimal growing conditions.
Ulmus laevis and U. glabra displayed particularly high
susceptibility to drought stress-induced cavitation (Table 3;
Fig. 5), so the expected aridification of the Iberian Penin-
sula (Somot et al. 2008; De Luis et al. 2010) could espe-
cially compromise the survival of their populations. As U.
glabra crossability with U. minor is high (Mittempergher
and La Porta 1991), it may potentially be adapted to more
xeric environments by means of hybridisation. Ulmus la-
evis is already critically endangered due to human habitat
transformation (Fuentes-Utrilla 2008; Venturas et al.
2013a), and is more vulnerable to aridification than U.
glabra due to its lower conductivities at declining water
potentials (Fig. 5b), and because it cannot hybridize with
U. minor (Mittempergher and La Porta 1991) to gain
drought resistance.
Summing up, hydraulic traits of the three European elms
growing in the Iberian Peninsula were shown in relation to
their habitats moisture gradients. Ulmus glabra and U.
minor showed tradeoffs between water transport efficiency
and xylem resistance to drought-induced cavitation, the
latter showing a hydraulic configuration that is better
adapted to overcome drought episodes. Ulmus laevis’
anatomy and hydraulic properties were favourable for
growing under high water availability, but they were highly
susceptible to drought-stress cavitation.
Acknowledgments We would like to thank Unai Lopez de Heredia,
Carmen Collada and Jesus Rodrıguez for their comments, and Eva
Miranda and Jorge Dominguez for their technical assistance. We are
grateful to Gerrie Seket for her language revision and to Salustiano
Iglesias for his support. We would also like to thank two anonymous
referees that have helped improve greatly this article with their com-
ments and suggestions. M.V. participation was possible thanks to a PIF
scholarship from the Technical University of Madrid. The project was
funded by the Comunidad de Madrid (project S2009AMB-1668).
References
Alder NN, Pockman WT, Sperry JS, Nuismer S (1997) Use of
centrifugal force in the study of xylem cavitation. J Exp Bot
48(3):665–674. doi:10.1093/jxb/48.3.665
Aref IM, Ahmed AI, Khan PR, El-Atta HA, Iqbal M (2013) Drought-
induced adaptive changes in the seedling anatomy of Acacia
ehrenbergiana and Acacia tortilis subsp. raddiana. Trees.
doi:10.1007/s00468-013-0848-2
Carlquist S (1977) Ecological factors in wood evolution: a floristic
approach. Am J Bot 64:887–896
Christman MA, Sperry JS, Adler FR (2009) Testing the ‘rare pit’
hypothesis for xylem cavitation resistance in three species of
Trees (2013) 27:1691–1701 1699
123
Author's personal copy
Acer. New Phytol 182:664–674. doi:10.1111/j.1469-8137.2009.
02776.x
Collin E (2003) EUFORGEN technical guidelines for genetic
conservation and use for European white elm (Ulmus laevis).
International Plant Genetic Resources Institute, Rome
Collin E, Bilger I, Eriksson G, Turok J (2000) The conservation of
elm genetic resources in Europe. In: Dunn CP (ed) The elms:
breeding, conservation, and disease management. Kluwer,
Boston, pp 281–293
Davis SD, Sperry JS, Hacke UG (1999) The relationship between
xylem conduit diameter and cavitation caused by freezing. Am J
Bot 86:1367–1372. doi:10.2307/2656919
De Luis M, Brunetti M, Gonzalez-Hidalgo JC, Longares LA, Martın-
Vide J (2010) Changes in seasonal precipitation in the Iberian
Peninsula during 1946–2005. Global Planet Change 74:27–33.
doi:10.1016/j.gloplacha.2010.06.006
Domec JC, Lachenbruch B, Meinzer FC, Woodruff DR, Warren JM,
McCulloh KA (2008) Maximum height in a conifer is associated
with conflicting requirements for xylem design. Proc Natl Acad
Sci USA 105:12069–12074. doi:10.1073/pnas.0710418105
Domec JC, Schafer K, Oren R, Kim HS, McCarthy HR (2010) Variable
conductivity and embolism in roots and branches of four
contrasting tree species and their impacts on whole-plant hydrau-
lic performance under future atmospheric CO2 concentration. Tree
Physiol 30:1001–1015. doi:10.1093/treephys/tpq054
Fuentes-Utrilla P (2008) Estudio de la variabilidad genetica del
genero Ulmus L. en Espana mediante marcadores moleculares.
Dissertation, Technical University of Madrid, Madrid
Gallego-Fernandez JB, Garcıa-Mora MR, Garcıa-Novo F (1999)
Small wetlands lost: a biological conservation hazard in
Mediterranean landscapes. Environ Conserv 26:190–199
Garcıa-Nieto ME, Genova M, Morla M, Rossignoli A (2000) Los
olmos en el paisaje vegetal de la Penınsula Iberica. In: Gil L,
Solla A, Iglesias S (eds) Los olmos ibericos. Conservacion y
mejora frente a la grafiosis. Organismo Autonomo Parques
Nacionales, Spain, pp 129–158
Giordano R, Salleo A, Salleo S, Wanderlingh F (1978) Flow in xylem
vessels and Poiseuille’s law. Can J Bot 56:333–338. doi:10.1139/
b78-039
Hacke UG, Jansen S (2009) Embolism resistance of three boreal
conifer species varies with pit structure. New Phytol
182:675–686. doi:10.1111/j.1469-8137.2009.02783.x
Hacke UG, Sauter JJ (1995) Vulnerability of xylem to embolism in
relation to leaf water potential and stomatal conductance in
Fagus sylvatica f. purpurea and Populus balsamifera. J Exp Bot
46:1177–1183. doi:10.1093/jxb/46.9.1177
Hacke UG, Sperry JS, Pittermann J (2000) Drought experience and
cavitation resistance in six shrubs from the Great Basin, Utah.
Basic Appl Ecol 1:31–41. doi:10.1078/1439-1791-00006
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001)
Trends in wood density and structure are linked to prevention of
xylem implosion by negative pressure. Oecologia 126:457–461.
doi:10.1007/s004420100628
Hacke UB, Sperry JS, Wheeler JK, Castro L (2006) Scaling of
angiosperm xylem structure with safety and efficiency. Tree
Physiol 26:689–701. doi:10.1093/treephys/26.6.689
Herbette S, Cochard H (2010) Calcium is a major determinant of
xylem vulnerability to cavitation. Plant Physiol 153:1932–1939.
doi:10.1104/pp.110.155200
Hultine KR, Koepke DF, Pockman WT, Fravolini A, Sperry JS,
Williams DG (2006) Influence of soil texture on hydraulic
properties and water relations of a dominant warm-desert
phreatophyte. Tree Physiol 26:313–323. doi:10.1093/treephys/
26.3.313
Jacobsen AL, Pratt RB, Davis SD, Ewers FW (2008) Comparative
community physiology: nonconvergence in water relations
among three semi-arid shrub communities. New Phytol
180:100–113. doi:10.1111/j.1469-8137.2008.02554.x
Jacobsen AL, Pratt RB, Tobin MF, Hacke UG, Ewers FW (2012) A
global analysis of xylem vessel length in woody plants. Am J Bot
99:1583–1591. doi:10.3732/ajb.1200140
Jansen S, Choat B, Pletsers A (2009) Morphological variation of
intervessel pit membranes and implications to xylem function in
angiosperms. Am J Bot 96:409–419. doi:10.3732/ajb.0800248
Jarbeau JA, Ewers FW, Davis SD (1995) The mechanism of water-
stress-induced embolism in two species of chaparral shrubs.
Plant Cell Environ 18:189–196. doi:10.1111/j.1365-3040.1995.
tb00352.x
Kolb K, Sperry JS (1999) Differences in drought adaptation between
subspecies of Sagebrush (Artemisia tridentata). Ecology 80:
2373–2384. doi:10.1890/0012-9658(1999)080[2373:DIDABS]
2.0.CO;2
Kozlowski TT (1997) Responses of woody plants to flooding and
salinity. Tree Physiol Monogr 1:1–29
Lens F, Sperry JS, Choat B, Christman MA, Rabaey D, Jansen S
(2011) Testing hypotheses that link wood anatomy to cavitation
resistance and hydraulic conductivity in the genus Acer. New
Phytol 190:709–723. doi:10.1111/j.1469-8137.2010.03518.x
Lopez R, Lopez de Heredia U, Collada C, Cano FJ, Emerson BC,
Cochard H, Gil L (2013) On vulnerability to cavitation,
hydraulic efficiency, growth and survival in an insular pine
(Pinus canariensis). Ann Bot (London) 111:1167–1179. doi:10.
1093/aob/mct084
Lovisolo C, Schubert A (1998) Effects of water stress on vessel size
and xylem hydraulic conductivity in Vitis vinifera L. J Exp Bot
49:693–700. doi:10.1093/jxb/49.321.693
MAGRAMA (2012) Database of the Ministry of Agriculture, Food
and Environment, Spain. http://sig.magrama.es/siga
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in
the vulnerability of woody plants to xylem cavitation. Ecology
85:2184–2199. doi:10.1890/02-0538
Mittempergher L, La Porta N (1991) Hybridization studies in the
Eurasian species of elm (Ulmus spp.). Silvae Genet 40:237–243
Nardini A, Salleo S, Lo Gullo MA, Pitt F (2010) Different responses
to drought and freeze stress of Quercus ilex L. growing along a
latitudinal gradient. Plant Ecol 148:139–147. doi:10.1023/A:
1009840203569
Pammenter NW, Van der Willigen C (1998) A mathematical and
statistical analysis of the curves illustrating vulnerability of
xylem to cavitation. Tree Physiol 18:589–593. doi:10.1093/
treephys/18.8-9.589
Pardos JA (2004) Respuestas de las plantas al anegamiento del suelo.
Invest Agrar: Sist Recur For, Fuera de Serie:101–107
Perry LG, Shafroth PB, Blumenthal DM, Morgan JA, LeCain DR
(2013) Elevated CO2 does not offset greater water stress
predicted under climate change for native and exotic riparian
plants. New Phytol 197:532–543. doi:10.1111/nph.12030
Philipson JJ, Coutts MP (1980) The tolerance of tree roots to water
logging. IV. Oxygen transport in woody roots of sitka spruce and
lodgepole pine. New Phytol 85:489–494. doi:10.1111/j.1469-
8137.1980.tb00763.x
Pittermann J, Sperry J (2003) Tracheid diameter is the key trait
determining the extent of freezing-induced embolism in conifers.
Tree Physiol 23:907–914. doi:10.1093/treephys/23.13.907
Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships
among xylem transport, biomechanics and storage in stems and
roots of nine Rhamnaceae species of the California chaparral.
New Phytol 174:787–798. doi:10.1111/j.1469-8137.2007.02061.
x
Raven JA (1996) Into the voids: the distribution, function, develop-
ment and maintenance of gas spaces in plants. Ann Bot
78:137–142. doi:10.1006/anbo.1996.0105
1700 Trees (2013) 27:1691–1701
123
Author's personal copy
Richens RH (1983) Elm. Cambridge University Press, Cambridge
Rodrıguez-Calcerrada J, Nanos N, Aranda I (2011) The relevance of
seed size in modulating leaf physiology and early plant
performance in two tree species. Trees 25:873–884. doi:10.
1007/s00468-011-0562-x
Rood SB, Braatne JH, Hughes FMR (2003) Ecophysiology of riparian
cottonwoods: stream flow dependency, water relations and
restoration. Tree Physiol 23:1113–1124. doi:10.1093/treephys/
23.16.1113
Rossignoli A, Genova M (2003) Corologıa y habitat de Ulmus glabra
Huds. en la penınsula Iberica. Ecologıa 17:99–121
Somot S, Sevault F, Deque M, Crepon M (2008) 21st century climate
change scenario for the Mediterranean using a coupled atmo-
sphere-ocean regional climate model. Global Planet Change
63:112–126. doi:10.1016/j.gloplacha.2007.10.003
Sorz J, Hietz P (2005) Gas diffusion through wood: implications for
oxygen supply. Trees 20:34–41. doi:10.1007/s00468-005-0010-x
Sperry JS (2003) Evolution of water transport and xylem structure. Int
J Plant Sci 164:S115–S127
Sperry JS, Tyree MT (1988) Mechanism of water stress-induced
xylem embolism. Plant Physiol 88:581–587. doi:10.1104/pp.88.
3.581
Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring
hydraulic conductivity and embolism in xylem. Plant Cell
Environ 11:35–40. doi:10.1111/j.1365-3040.1988.tb01774.x
Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency
conflicts in hydraulic architecture: scaling from tissues to trees.
Plant Cell Environ 31:632–645. doi:10.1111/j.1365-3040.2007.
01765.x
Sperry JS, Christman MA, Torres-Ruiz JM, Taneda H, Smith DD
(2012) Vulnerability curves by centrifugation: is there an open
vessel artefact, and are ‘r’ shaped curves necessarily invalid?
Plant Cell Environ 35:601–610. doi:10.1111/j.1365-3040.2011.
02439.x
Swift CC, Jacobs SM, Esler KJ (2008) Drought induced xylem
embolism in four riparian trees from the Western Cape Province:
insights and implications for planning and evaluation of
restoration. S Afr J Bot 74:508–516. doi:10.1016/j.sajb.2008.
01.169
Tissier J, Lambs L, Peltier JP, Marigo G (2004) Relationships
between hydraulic traits and habitat preference for six Acer
species occurring in the French Alps. Ann For Sci 61:81–86.
doi:10.1051/forest:2003087
Tobin MF, Pratt RB, Jacobsen AL, De Guzman ME (2012) Xylem
vulnerability to cavitation can be accurately characterised in
species with long vessels using a centrifuge method. Plant Biol
15:496–504. doi:10.1111/j.1438-8677.2012.00678.x
Tsuda M, Tyree MT (1997) Whole-plant hydraulic resistance and
vulnerability segmentation in Acer saccharinum. Tree Physiol
17:351–357. doi:10.1093/treephys/17.6.351
Tyree MT, Sperry JS (1988) Do woody plants operate near the point
of catastrophic xylem dysfunction caused by dynamic water
stress? Answers from a model. Plant Physiol 88:574–580. doi:10.
1104/pp.88.3.574
Tyree MT, Zimmerman MH (2002) Xylem structure and the ascent of
sap, 2nd edn. Springer-Verlag, New York
Tyree MT, Cochard H, Cruiziat P, Sinclair B, Ameglio T (1993)
Drought-induced leaf shedding in walnut: evidence for vulner-
ability segmentation. Plant Cell Environ 16:879–882. doi:10.
1111/j.1365-3040.1993.tb00511.x
Tyree MT, Kimberley JK, Rood SB, Patino S (1994) Vulnerability to
drought-induced cavitation of riparian cottonwoods in Alberta: a
possible factor in the decline of the ecosystem? Tree Physiol
14:455–466. doi:10.1093/treephys/14.5.455
Vander Willigen C, Sherwin HW, Pammenter NW (2000) Xylem
hydraulic characteristics of subtropical trees from contrasting
habitats grown under identical environmental conditions. New
Phytol 145:51–59. doi:10.1046/j.1469-8137.2000.00549.x
Venturas M, Fuentes-Utrilla P, Ennos R, Collada C, Gil L (2013a)
Human induced changes on fine-scale genetic structure in Ulmus
laevis Pallas wetland forests at its SW distribution limit. Plant
Ecol 214:317–327. doi:10.1007/s11258-013-0170-5
Venturas M, Lopez R, Martın JA, Gasco A, Gil L (2013b) Resistance
to Dutch elm disease in Ulmus minor is heritable and related to
xylem vessel size but not vulnerability to cavitation. Plant
Pathol. doi:10.1111/ppa.12115
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel
pitting and cavitation in woody Rosaceae and other veselled
plants: a basis for a safety vs. efficiency trade-off in xylem
transport. Plant Cell Environ 28:800–812. doi:10.1111/j.1365-
3040.2005.01330.x
Wiegrefe S, Sytsma KJ, Guries RP (1994) Phylogeny of elms (Ulmus,
Ulmaceae): molecular evidence for a sectional classification.
Syst Bot 19:590–612
Yamamoto F, Angeles G, Kozlowski TT (1987) Effect of ethrel on
stem anatomy of Ulmus americana seedlings. IAWA Bull 8:3–9
Trees (2013) 27:1691–1701 1701
123
Author's personal copy
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