Water relations and hydraulic characteristics of three woody species co-occurring in the same habitat
Ann. For. Sci.
Water relations and hydraulic characteristics of three woody species co-occurring in the same habitat
Andrea NARDINI 1
Sebastiano SALLEO 1
Patrizia TRIFILÒ 1
Maria Assunta LO GULLO 0
0 Dipartimento di Scienze Botaniche, Università di Messina , Salita Sperone 31, 98166 Messina S. Agata , Italy
1 Dipartimento di Biologia, Università di Trieste , Via L. Giorgieri 10, 34127 Trieste , Italy
- Three woody species typically encroaching the Karstic region of Trieste (Northeastern Italy) i.e. Cotinus coggygria L., Prunus mahaleb L. and Fraxinus ornus L., have been measured for diurnal and seasonal time courses of leaf conductance to water vapour, transpiration and water potential ( L), as well as whole-plant, shoot and root hydraulic resistance (Rplant, Rshoot and Rroot, respectively) in view of investigating the impact of plant hydraulics on water stress resistance. F. ornus suffered the highest L drop in July and September due to the high Rplant measured in this species. Positive significant relations were found of Rplant and L to Rroot in all three species studied, thus suggesting that root hydraulics is a major determinant of plant hydraulics and water stress resistance. The increasing Rroot (and Rplant) from C. coggygria to P. mahaleb to F. ornus provided a possible explanation for the typical temporal sequence of expansion of the three species into degraded areas.
The concept of “hydraulic architecture” of plants was first
introduced by M. Zimmermann [
] in view of relating the
structure and physical properties of the water conducting
system to plant water balance and adaptation to the
environment. In this framework, the partitioning of the
hydraulic resistances (R) along the plant body and their
seasonal changes are of particular interest and, in fact,
Zimmermann and co-workers have discussed extensively the
possible evolutive and adaptive significance of changes in the
hydraulic conductance (K = 1/R) of stems and leaves of
several tree species [
]. During the last two decades, our
knowledge of the hydraulic architecture of plants has been
enriched with accurate measurements of the hydraulic
resistance of the root (Rroot) whose dominant component (by
85 to 95%) has revealed to reside in the radial pathway
between the soil and the root stele [
]. In turn, the overall
shoot resistance (Rshoot) has been reported to be dominantly
located in the leaf blade (Rleaf) i.e. leaves would account for
50 to 90% of the measured Rshoot [
19, 21, 40
]. On the basis of
the above, a plant might be viewed as consisting of two
opposite poles i.e. the leaf and the radial soil-to-root stele
pathway, both characterized by high R’s and connected to one
another by a low-R pathway (the xylem). This last water path,
however, can increase its own R by a factor of two or more due
to cavitation . A convincing body of evidence, in fact, has
accumulated showing that xylem cavitation takes place in
conduits whenever tensions in them exceed critical thresholds
so that gaseous microbubbles are sucked into conduits leading
to their embolism and blockage [
34, 41, 44
]. Some of the
several species studied for cavitation so far, however, have
shown to recover from xylem embolism at least partly, as
transpiration declines and even in presence of active
] in a matter of minutes [
] or hours .
According to the Ohm’s law hydraulic analogue, the
hydraulic resistance of a plant (Rplant) is positively related to
the driving force for the flow corresponding to the water
potential ( ) difference between the soil and leaf ( soil – L)
Rplant = ( soil –
L) / F,
where F is the flow through the plant. Because the root and the
shoot are serial components in a plant,
Under sufficient water availability, the hydraulic resistance of
the root is 50 to 60% of that of the whole plant [
Rplant = Rroot + Rshoot.
During water shortage conditions, however, as well as under
freeze or salinity stress, Rplant can increase significantly in
both its components (Rroot and/or Rshoot, [
4, 14, 16, 25
particular, Rroot may increase due to root cavitation [
and/or to the new formation of a multi-layer suberized
endoderm-like tissue that hydraulically isolates the stele from
the cortex [
5, 12, 16, 23
]. In turn, Rshoot can be enhanced by
stem and leaf vein cavitation [
] and stomatal closure [
]. Sperry et al.  have developed a model showing that
plant water use is mainly limited by the efficiency of the xylem
and only to a lesser extent by the rhizosphere. Nardini et al.
], on the other hand, reported that the decrease in leaf
conductance to water vapour (gL) and water potential ( L)
recorded in Quercus species during Sicilian summers were
paralleled by opposite changes in Rroot. Now, the question
arises whether the major contribution to the increase in Rplant
under stress conditions is due to Rroot or Rshoot. Answering
this question has both theoretical and practical interest because
the recovery of the hydraulic efficiency of the shoot i.e. xylem
refilling and stomatal re-opening, is likely to require less
metabolic investment by the plant than that of the root at least
in the case new roots have to be produced to substitute for
those no longer in hydraulic continuity with the soil [
In view of investigating possible relationships existing
between changes in hydraulic resistance of plants and their
adaptation to the environment, in the present study we report
daily and seasonal measurements of water relation parameters
as well as of root and shoot hydraulic resistance in three
fieldgrowing species co-occurring in the same habitat i.e. Cotinus
coggygria L. (Wig tree), Prunus mahaleb L. (Mahaleb cherry)
and Fraxinus ornus L. (Manna ash). These species are
dominant components of the vegetation developing during the
natural encroachment of abandoned rural areas in the Karstic
region (Friuli-Venezia Giulia, Northeastern Italy). The Karstic
areas are characterized by high soil drainage [
] so that even
in presence of sufficient annual rainfall, plants may suffer
summer (and winter) water stress [
]. The dynamic sequence
of expansion of the three species above into the area sees
C. coggygria settling first, followed by P. mahaleb and some
years later, by F. ornus [
9, 10, 24
]. A previous study of some
of us [
] had shown that the co-occurrence of two
Mediterranean Quercus species (Q. suber L. and Q. cerris L.)
in Sicily could be explained in terms of their complementary
changes in Rroot through the year that allowed the peaks of
their water demand to be reached in different periods of the
year. Therefore, a second objective of our study was to check
whether the co-occurrence of C. coggygria, P. mahaleb and
F. ornus might be explained on the basis of different
hydraulics and adaptive strategies.
2. MATERIALS AND METHODS
2.1. The study site
The study site was located near the village of Basovizza in the
Karstic area of Trieste at an altitude of about 300 m. The soil in this
area is a poorly developed brown soil with rather low water retention
] and the typical climate has been defined as a pre-Alpine
continental climate. Mean rainfall is about 1150 mm with a maximum
in autumn and a minimum in winter (between January and March).
Winter temperatures often fall below 0 °C and in the coldest month
(January) the mean of the daily minima is, on average, 2.9 °C (data
from the Oceanography and Meteorology Section, Dept. of Earth
Sciences, University of Trieste). The vegetation in the study site
consisted of well developed shrubs of C. coggygria mixed with
P. mahaleb and F. ornus trees as dominant species. Other
cooccurring woody species were: Crataegus monogyna, Rosa canina,
Q. pubescens, Acer monspessulanum, Juniperus communis and Pinus
nigra ( and personal observations).
2.2. Measurements of plant water status and hydraulics
The diurnal time course of leaf conductance to water vapour (gL),
transpiration rate (EL) and water potential ( L) was recorded every
60 min between 0630 h (pre-dawn) and 1830 h solar time, in selected
sunny days of May (23 to 25), July (26 to 28) and September (12 to
15) 2000. These months were selected for measurements because
previous studies [
] had shown that although the spring is
usually rainy in Venezia Giulia, plants suffer some loss of hydraulic
conductance due to winter embolism while July is the warmest month
and September is usually preceded by a dry period (August) and
coincides with the beginning of processes leading to leaf senescence.
Measurements were performed on three adult individuals of each
species with an estimated age of 15–20 years. The same individuals
were measured for the above variables in May, July and September.
Samples for measuring leaf water status and gas exchange (see
below) were sun leaves collected from the S-exposed part of the
Leaf conductance to water vapour and transpiration rate were
measured of at least 15 leaves per species and per daytime using a
portable steady-state porometer (LI1600, LiCor Inc., Lincoln, NE,
USA). Air temperature (Tair), relative humidity (RH) and
photosynthetically active radiation (PAR) were also recorded using
the porometer cuvette, at about 1 m from the S-exposed part of the
crown. Leaf water potential ( L) was measured of six to ten leaves
per species and per daytime using a portable pressure chamber (3005
Plant Water Status Console, Soilmoisture Equipment Corp., Goleta,
CA, USA) with sheets of wet filter paper inside the chamber to
minimize water loss during measurements.
In order to estimate seasonal changes in L at the turgor loss point
( TLP), pressure-volume curves [
] of four to five leaves per
species and per study period were measured. The turgor loss point
served as a reference point for estimating the residual turgor of leaves
when reaching the minimum diurnal L . So as to quantify the
overall diurnal drop in L, the integral of L was calculated between
two reference daytimes i.e. predawn and sunset when L is least
negative. We named this variable “Water Stress Index” or WSI [
In other words:
where t0 and tx are predawn and sunset times, respectively and dt is
the time interval during which L was measured. This L expression
was first proposed by Mishio and Yokoi [
] and has proved to be a
more reliable indicator of the amount of water stress suffered by
] with respect to other common variables used to the same
purpose like minimum L or the difference between pre-dawn and
minimum diurnal L.
An estimate of the seasonal changes in the hydraulic resistance (R)
of plants (Rplant) as well as of that of the root system (Rroot) and shoot
(Rshoot) was obtained using the “evaporative flux” method (EF)
which is based upon the Ohm’s law hydraulic analogue i.e.
Rplant = ( pd –
Rroot = ( pd –
Rshoot = ( x –
where pd is pre-dawn L which is assumed to equilibrate to soil
water potential i.e. soil pd [
], min is the minimum diurnal L
as measured at midday and EL is the midday transpiration rate. The
term x represents the water potential of xylem at the trunk base.
This was estimated by covering four to five leaves growing near the
base of plants with plastic film and aluminum foil before sunrise.
Under these conditions, leaf water potential is generally agreed to
equilibrate to that of the adjacent xylem [
]. The covered leaves
were collected at midday and measured for L. Midday values of L,
x and EL were preferred because at this daytime plants are likely to
have transpired all their stored water so that steady-state water flow
conditions are likely to establish.
In other words, because pd is assumed to equilibrate with soil
(which is the case for not really arid soils), ( pd – min) in equation 5
would represent the water potential difference driving the flow from
the soil to the leaf (at midday). In turn, ( pd – x) in equation 6
would be the driving force for the flow from the soil to the trunk base
and ( x – min) in equation 7 would be that between the trunk base
and the leaf.
We are aware that in many cases pd may not equilibrate with
], so that measuring soil, directly would be more correct.
However, Karstic soils are characterized by deep fissures in the rocky
subsoil into which roots may penetrate, so that measuring the water
potential of a soil sample is likely to provide false information of the
water potential actually experienced by plant roots. In these cases,
estimating soil on the basis of pd is preferable and pd represents
the maximum (i.e., least negative) water potential plants can reach
under given conditions.
The annual time course of air temperatures (Tair) and
precipitation (Fig. 1, data from the Oceanography and
Meteorological Section, University of Trieste for the year
2000, recorded about 1 Km from the study site) was
characterized by a typically arid and cold winter (mean Tair
dropped to –6 °C and only about 10% of annual precipitation
was recorded between January and March). Two peaks of
precipitation were recorded in the course of year 2000, one of
which occurred in July i.e. about one month later with respect
to the mean of the last 30 years, and a second one, in
November. Therefore, measurements of plant water status in
July were made during a warm, wet period. In September, on
the contrary, plants received scarce rainfall (and in August as
well, Fig. 1) while air temperatures were still high (mean Tair
was over 20 °C).
3.1. Changes in plant water status
The diurnal time courses of gL, EL and L as measured in
the three species under study are reported in Figures 2, 3 and
4. Changes in gL and EL as recorded in May, July and
September were qualitatively similar in C. coggygria,
P. mahaleb and F. ornus, the largest midday gL and EL being
recorded in July (gL was 200 to 250 mmol m–2 s–1) and the
lowest values being recorded in September (gL was 75 to
100 mmol m–2 s–1). In all the three species and year periods
studied, EL paralleled gL. The three species differed, however,
for their L time courses. In C. coggygria, L decreased
progressively from May to September (Fig. 2) both in terms of
min (from –1.0 to –2.0 MPa) and in terms of pd (from –0.4
to –1.1 MPa). It can be noted, however, that the L time
course recorded in May was, in this species, not very different
from that recorded in July.
The seasonal decrease in L was slightly smaller in
P. mahaleb with respect to that measured in C. coggygria in
that min decreased only from –1.2 to –1.8 MPa from May to
September and pd from –0.4 to –0.6 MPa in the same time
interval. It has to be noted that the lowest diurnal L values
recorded in July in this species recovered promptly while they
were maintained for several hours in September (from 0930 to
1600 h, Fig. 3) and recovered only during the night.
The diurnal time course of L in F. ornus was
quantitatively different from that recorded in the other two
species (Fig. 4). The strong reduction in gL and EL (by a factor
of over three) recorded in September with respect to values
recorded in July, was paralleled by L dropping to –3.5 MPa
and reaching the turgor loss point ( tlp). Such a low L level
was more or less maintained during the warmest hours of the
day i.e. between 1000 and 1600 h but it recovered in the
afternoon. In the same month, also pd was found to drop
substantially i.e. it became threefold more negative than that
recorded in May and July. Although July 2000 was
characterized by unusually high precipitation (Fig. 1), L of
F. ornus dropped to –2.3 MPa, a level approaching the turgor
loss point ( tlp was –2.5 MPa).
Figures 2, 3 and 4 show that the minimum diurnal L
values were either promptly recovered or maintained during
the warmest hours of the day. In this last case, the total
“pressure” acting on plant metabolism due to decreased water
status can be better estimated in terms of WSI that takes into
proper account the duration of the minimum L levels and
also the extent to which pd actually decreased. WSI as
calculated for C. coggygria and P. mahaleb was of the order
of 8 to 9 MPa h for the former species and 12 to 14 MPa h for
the latter in May and July, but increased significantly in
September when WSI increased twofold in C. coggygria i.e.
from about 9 to 18 MPa h (Fig. 5). In P. mahaleb, meanwhile,
the increase in WSI from the spring to late summer was of the
order of only about 38% (from 13 to 18 MPa h). The largest
changes in WSI were recorded in F. ornus, however, where the
integral of L between predawn and sunset increased
significantly in July, already (from about 12 to 18 MPa h, i.e.,
by 50%) and much more in September when it was found to
be of the order of about 35 MPa h i.e. three times higher than
that calculated in May.
3.2. Partitioning of hydraulic resistances
Seasonal changes in Rplant and its components (Rroot and
Rshoot) are reported in Figure 6. The whole plant hydraulic
resistance (Rplant, white columns) changed in a qualitatively
similar way in the three species under study. In fact, Rplant was
found to decrease in July with respect to May but to increase
substantially in September. In the spring, the lowest Rplant was
recorded in C. coggygria (about 1.0 104 MPa s m2 kg–1) and
the highest one, in F. ornus (about double). Rplant as recorded
in July was in every case, of the order of 20 to 30% less than
that measured in May. In September, Rplant was about twice as
much as that measured in the spring in C. coggygria and
P. mahaleb and 2.4 times more in F. ornus. In turn, Rshoot
(dashed columns, Fig. 6) was significantly larger than Rroot
(black columns) in May, in all species studied. In July, the
relative contribution of Rshoot to Rplant became smaller so that
Rshoot became approximately equal to Rroot in C. coggygria
and F. ornus (about 0.25 and 0.8 104 MPa s m2 kg–1,
respectively) while Rshoot was only about one third of Rroot in
P. mahaleb (Rshoot and Rroot were about 0.2 and 0.7 104 MPa
s m2 kg–1, respectively). In September, Rshoot contributed
rather little to Rplant (only 10% in P. mahaleb and about one
third in C. coggygria and F. ornus).
The impact of Rroot on Rplant is described in Figure 7 where
all Rroot values recorded in the three species and year periods
under study were plotted versus the corresponding Rplant
values. The two variables resulted to be positively and linearly
related to one another with a correlation coefficient as high as
0.91 and with a significance of P < 0.0001. The overall
resistance of the root system (Rroot) appeared to be also
linearly and positively related to WSI (Fig. 8). The overall
diurnal drop in L (WSI) increased in response to the increase
in Rroot, in all species studied, with a coefficient of about 0.80
and a significance of P < 0.01.
The three species under study did not differ much for
seasonal patterns of gL, EL or RWC (Figs. 2, 3 and 4). At least
two significant differences among species, however, emerged
in terms of seasonal changes in the L time course. Primarily,
diurnal Ls recorded in C. coggygria and P. mahaleb did not
approach their respective leaf turgor loss points in any of the
periods studied i.e., leaves of the two species maintained their
turgor even through the summer period. Leaves of F. ornus,
meanwhile, not only showed Ls dropping very near to their
tlp in July already but reached tlp in September when leaf
turgor was lost for several hours during the day (Fig. 4), in
spite of consistent stomatal closure i.e., at low gL. Secondly,
the environmental pressure acting on plants, expressed here as
the overall diurnal drop in L (WSI, Fig. 5) was impressively
high in F. ornus when compared to that estimated for the other
two species (in July and September, WSI in F. ornus was
about twice higher than that recorded for C. coggygria).
Because the three species studied are deciduous and most trees
in the study area initiate the processes leading to leaf
senescence in late summer already [
], the lower leaf water
status recorded in September with respect to May (and July)
may be interpreted as the expression of the beginning of leaf
senescence that has been reported to imply the loss of
hydraulic efficiency of petioles and stems [
]. An alternative
explanation, however, is that the L drop recorded in
September in all the species studied was the consequence of
the water limitation suffered by plants in August when only
20 mm precipitation were recorded. In fact, water limitation
accompanied by high temperatures (Fig. 1) is well known
to lead to xylem embolism and impair of xylem water
The overall plant hydraulic resistances (Rplant) were quite
different in the three species studied (Fig. 6). In May, Rplant of
F. ornus was twice as much as that recorded in C. coggygria
and 25% more than Rplant of P. mahaleb. Such differences
tended to increase in July and further in September when
Rplant of F. ornus was 2.2 times more than that of C. coggygria
and 58% more than that recorded in P. mahaleb. This suggests
that differences in Rplant among species are dependent on their
root, stem and leaf anatomy and they also depend on the
ongoing functional losses by plant organs in terms of water
transport efficiency. The decrease of Rplant recorded in July
with respect to May in all the three species studied, was more
due to the proportional decrease in Rshoot than to changes in
Rroot which changed not much (Fig. 6). In principle, Rshoot
consists of the two serial components represented by stem and
leaves i.e. Rshoot = Rstem + Rleaf. The hydraulic resistance of a
stem can be expected to decrease as a consequence of cambial
activity leading to the new production of wide conduits that
contribute most to the flow [
] and, hence, to hydraulic
conductance. In our opinion, the lower Rshoot recorded in July
with respect to May can be interpreted as due to new xylem
conduits produced between the end of May and July
corresponding to the rhythm of stem growth reported by
] and Evert [
]. Previous studies by some of us had
provided evidence that loss of hydraulic conductance (PLC) of
stems of some both deciduous and evergreen trees in Friuli
Venezia Giulia was typically high in the winter, persisted
partly in May and was recovered only in July. As an example,
PLC measured in Quercus pubescens Willd. was as high as
about 70% in May and dropped to 40% in July [
Quercus ilex L., PLC was about 35% in May and 10% in
The noticeable increase in Rplant recorded in September for
the three species under study was mostly due to Rroot that
represented 70 to 90% of Rplant. Several studies have reported
consistent increases in Rroot as a consequence of water stress
5, 12, 23
] stimulating the new formation of an endoderm-like
multilayer of suberized cells interrupting the hydraulic
continuity between soil and the root stele [
]. The impressive
increase in Rroot in September provides, in our opinion, a good
although circumstantial explanation for the significant
increase in WSI recorded in all the species studied, in the same
month with respect to May as well as that recorded in F. ornus
in July, already. Because Rroot as derived on the basis of
equation 6 includes the resistance of the soil-to-root pathway,
it is possible that the measured Rroot was due to the increase of
Rsoil. In turn, Rsoil is negligible when soil water content and
soil are high. In our case, however, soil as estimated on
the basis of pd was always below –0.3 MPa and as low as
–1.6 MPa for F. ornus in September. This suggests that Rsoil
was not constant for the three species and for the three study
periods. The differences recorded between species in terms of
pd also suggest that contrasting behaviors between species
might be due to different rooting patterns. However, this is
only a tentative explanation because we do not have any
information about the rooting depth of the species studied. It
has to be taken into account that this important aspect of plant
adaptation is difficult to assess because of the extensive
outcropping rocks typical of Karstic soils.
Over the entire study period, the whole-plant hydraulic
resistance appeared to be strongly related to Rroot (Fig. 7). The
close correlation between the two, confirms the root as an
organ highly sensitive to changes in environmental factors like
temperature and water availability as well as to plant growth
rhythms. This is in accordance with several recent studies
attributing to roots a major role in determining the whole-plant
water balance [
6, 23, 35
]. In our case, in fact, the diurnal drop
in L was related to Rroot with a close correlation between the
two variables. In this view, hydraulic measurements can
significantly implement measurements of classic water
relation parameters like L, RWC and others and provide a
more extensive understanding of their short-term and
The typical dynamic sequence of encroachment of
abandoned grazing areas of the Karstic region [see above and
9, 10, 24] is in accordance with stress resistance strategies of
the three species under study. In this regard, C. coggygria
behaved like a drought resistant species combining high leaf
gas exchange with rather low L changes both in the spring
and midsummer (Figs. 1 and 5). This was likely to be the result
of constantly low Rroot’s (less than 0.5 104 MPa s m2 kg–1)
that allowed efficient water absorption and transport to leaves.
Such highly efficient plant hydraulics might provide an
explanation, in our opinion, of the rapid expansion of this
species into abandoned degraded areas. We are aware that
hydraulic architecture is only one of the factors which confer
competitivity to pioneer species. Differences in height, leaf
arrangement, crown shape, carbon allocation to roots versus
leaves or root development, all are known to affect plant
growth rate with respect to competitors. These factors were
not taken into account in the present study, so our
interpretation of the adaptive advantage of efficient plant
hydraulics has to be taken as tentative. The significantly
higher (about double) Rroot and Rshoot recorded in F. ornus
both in May and in July (Fig. 4) caused leaves of this species
to approach turgor loss point during the warm period i.e. to
make the species less competitive than C. coggygria (and
P. mahaleb) for water and nutrient availability. The major
vulnerability to water stress exhibited by F. ornus with respect
to the other two species helps to explain why F. ornus expands
into abandoned areas only border on newly encroached
] where competition with other species is less critical
and microclimatic factors are more favorable.
In conclusion, we feel that a more complete view of plant
adaptation to the environment can emerge from a hydraulic
description of plant organs which also allows to better
interpret future possible trends in the restoration of degraded
Acknowledgements: The present study was funded by Italian Ministry
for University and for Scientific and Technological Research, in the
frame of the National Project “Biodiversità e processi di recupero
della vegetazione nelle aree marginali” (MURST Cofin 1998). We
are grateful to Dr Fabio Raimondo for assistance during field
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