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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

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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

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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

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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-

a

a b

b

b

b a

b

b

b

a

aa a

c

b

a

a

aa a

0

10

20

30

40

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).

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