ARTICLE IN PRESS

Journal of Theoretical Biology 249 (2007) 111123

www.elsevier.com/locate/yjtbi

A model of bubble growth leading to xylem conduit embolism

T. Holttaa,, T. Vesalab, E. Nikinmaac
a

School of GeoSciences, Crew Building, University of Edinburgh, West Mains Road, EH9 3JN Edinburgh, UK
b
Department of Physical Sciences, University of Helsinki, P.O. Box 64, FIN-00014 Helsinki, Finland
c
Department of Forest Ecology, University of Helsinki, P.O. Box 24, FIN-00014 Helsinki, Finland
Received 29 March 2007; received in revised form 18 May 2007; accepted 24 May 2007
Available online 2 June 2007

Abstract
The dynamics of a gas bubble inside a water conduit after a cavitation event was modeled. A distinction was made between a typical
angiosperm conduit with a homogeneous pit membrane and a typical gymnosperm conduit with a torusmargo pit membrane structure.
For conduits with torusmargo type pits pit membrane deection was also modeled and pit aspiration, the displacement of the pit
membrane to the low pressure side of the pit chamber, was found to be possible while the emboli was still small. Concurrent with pit
aspiration, the high resistance to water ow out of the conduit through the cell walls or aspirated pits will make the embolism process
slow. In case of no pit aspiration and always for conduits with homogeneous pit membranes, embolism growth is more rapid but still
much slower than bubble growth in bulk water under similar water tension. The time needed for the embolism to ll a whole conduit was
found to be dependent on pit and cell wall conductance, conduit radius, xylem water tension, pressure rise in adjacent conduits due to
water freed from the embolising conduit, and the rigidity and structure of the pits in the case of margotorus type pit membrane. The
water pressure in the conduit hosting the bubble was found to occur almost immediately after bubble induction inside a conduit, creating
a sudden tension release in the conduit, which can be detected by acoustic and ultra-acoustic monitoring of xylem cavitation.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: Embolism formation; Bordered pits; Bubble growth; Pit aspiration

1. Introduction
According to the cohesion-tension theory water ow in
plants is driven by water evaporation at the leaf surfaces,
which creates a pull of a continuous water column through
the xylem (Zimmermann, 1983). Water is regularly in a
meta-stable state, where its pressure has dropped below
saturation vapor pressure (Nobel, 1991). Under these
conditions the water columns are vulnerable to cavitation
by formation of gas bubbles from air seeding, i.e. air
penetration from adjacent conduits or air spaces through
little pores, or by actual phase transition through heterogeneous nucleation (e.g. Pickard, 1981; Tyree, 1997). These
processes induce a gas phase large enough for the
volumetric expansion energy to overcome the surface
energy needed to make the new gas/liquid interface, and
the bubble is able to grow (Brennen, 1995).
Corresponding author. Tel.: +44 131 650 5427; fax: +44 131 662 0478.

E-mail address: teemu.holtta@ed.ac.uk (T. Holtta).

0022-5193/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jtbi.2007.05.033

In a liquid under tension, unrestricted by solid boundaries, a bubble above a critical size would grow
explosively, in a fraction of a second, to ll the volume
of an individual xylem water conduit (Brennen, 1995).
However, a gas bubble expanding in a xylem conduit has to
displace water volume in the conduit as it grows, and the
relatively inelastic lignied walls of the conduit resist the
volumetric expansion of the conduit. At the same time, the
outow of liquid water out of the conduit is restricted by
the hydraulic resistance of the conduit lumen itself and the
bordered pits through which water is exchanged with
neighboring xylem conduits.
The stability of gas bubbles in the xylem in connection to
cavitation has been modeled (e.g. Shen et al., 2002), but the
dynamics of the bubble growth inside a xylem conduit has
not received much attention. The dynamics of bubble
growth inside a xylem conduit has not been modeled
before, and the only observation of embolism dynamics
from the literature, as far as we know, is the study of
Lewis et al. (1994), where full embolism in the tracheids of

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T. Holtta et al. / Journal of Theoretical Biology 249 (2007) 111123

Thuja occidentalis L. was found to occur in approximately

5 min after embolism induction. In this study we model the
growth of the gas bubble inside a xylem water conduit
following cavitation. A distinction is made between a
conduit with a homogeneous pit membrane typically found
in angiosperms and a conduit with a torusmargo pit
found in gymnosperms. For the later, pit aspiration and its
effect on embolism formation is also taken into account.
Bordered pits are small circular regions in the conduit
wall in which the secondary wall is missing (Siau, 1984).
Bordered pits consist of a pit chamber and a pit membrane
through which water ow among adjacent water conduits
takes place (Taiz and Zeiger, 1998). The pit membrane
structure of gymnosperms and angiosperms is different.
Angiosperms have usually homogeneous pit membranes,
which must allow water passage through them and at the
same time prevent the passage of air by trapping airwater
meniscus by capillary action (Sperry and Hacke, 2004).
Gymnosperm pit membrane has usually a more complicated structure (Hacke et al., 2004), in which the closing
membrane is made up of a thick central region, torus, and a
thin peripheral region, margo. The torus is relatively
impermeable to water ow, while the margo is perforated
and much more permeable to water ow (Siau, 1984).
The function of the pit membrane is to block the passage
of air from embolised conduits to water lled ones, thus
preventing the spreading of embolisms. The airwater
interface between an embolised and a functioning conduit
resides to the pores of the pit membrane (Zimmermann,
1983). The pressure difference in the water and air phases
over the membrane exerts a force to stretch the microbril
strands that are holding the membrane in place, and the
membrane is deected to the low pressure side of the pit
chamber (e.g. Petty, 1972, Hacke et al., 2004, Sperry and
Hacke, 2004). However, if the pressure difference over the
pit membrane grows larger than the surface tension forces
needed to maintain the liquidgas interface intact, air is
seeded from the embolised conduit to the adjacent conduit
and the embolism spreads. The size of largest individual
pore of in the pit membranes separating a water lled
conduit from an embolised is thought to determine the
maximum pressure difference that can exist over the
membrane without the induction of air-seeding (Tyree,
1997).
The pit membrane should also be displaced when
another type of force, other than that caused by surface
tension over the airwater interface in the membrane, is
acting on it. Induction of a large pressure difference in
liquid water between two adjacent conduits should also
cause pit membrane deection by creating a hydrostatic
force on the pit membrane. However, in normal transpiration driven water ow situation the pressure difference over
the membrane is far too small to displace the pit membrane
considerably and cause pit aspiration (Gregory and Petty,
1973). Bolton and Petty (1978) and Chapman et al. (1977)
have modeled the deection of torusmargo type gymnosperm pit membrane in the presence of a much larger water

ux between two conduits than that resulting from

transpiration driven water ow. Both studies came to the
conclusion that torusmargo type pits act like valves,
permitting only moderate water uxes through them as
with large water uxes the torus blocks the pit opening and
no water will ow through the pit. Sperry and Tyree (1990)
found experimentally that the hydraulic conductivity of
gymnosperm wood samples decreased as the pressure
gradient used to drive water through the samples increased
much above transpiration-induced values. Pit aspiration
was hypothesized as the reason for this drop in hydraulic
conductivity. Also Hammel (1967) and Robson et al.
(1988) proposed that a large liquid pressure difference
between two conduits would cause pit aspiration of a
torusmargo pit, but in the case of a partly frozen and an
unfrozen xylem tracheid. As we show later in this study,
large water pressure differences and temporarily large
water uxes will be developed between adjacent conduits in
connection to embolism formation. For gymnosperms
with torusmargo type pits this could induce the closed
valve type behavior as described above, whereas for
angiosperms with homogeneous pit membranes, pit
membrane deection would have only little effect on the
functioning of the pit.
The dynamics of a gas bubble inside a xylem water
conduit are calculated here using numerical methods to
solve the equations associated with the gas phase growth,
water ow out of a conduit hosting the growing bubble,
water pressure development, and also the transient pit
conductance for the torusmargo structure pits. The time
required for a gas bubble to completely ll an embolising
conduit is calculated for varying conduit structures and
xylem tensions. The time-scale needed to drain a conduit of
water is also interesting in view of the possible embolism
and embolism relling cycles. Experimental studies
have shown that embolisms are frequently relled, and
some studies have even observed relling during relatively
high transpiration (Melcher et al., 2001; Tyree et al.,
1999; Canny, 1997). If a conduit would not be fully drained
of water before relling commences, it could also be
easier and faster to rell. The dynamics of bubble growth is
also interesting from the perspective of the detection of
acoustic and ultra-acoustic sonic emissions, which are
observed concurrently with cavitation events (e.g. Milburn
and Johnson, 1966; Tyree and Dixon, 1983). It is not
completely clear what exactly gives rise to these emissions
(Jackson and Grace, 1996).
2. Theory
Here we describe how the dynamics of the bubble/gas
phase in an embolising conduit is described in its different
phases in the calculations. Fig. 1 depicts an outline of the
different phases of a bubble/gas phase growing in a conduit
for a tree with torusmargo type pit membranes. Fig. 1A
shows the initial stage of the process where a critical size
bubble has been induced inside the conduit lumen and the

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113

In Fig. 1C the gas phase has reached the radius of the

conduit and is no longer spherical. The gas phase spreads
towards the tapered ends of the conduit. The pits remain
aspirated. However, pit aspiration does not occur at all if
the pressure difference over the pit membrane does not
grow high enough to overcome the elastic forces in the
margo strands, or alternatively pit aspiration can also
occur after the gas phase has reached the conduit diameter
size. For angiosperms conduits with homogeneous pit
membranes, pit membrane deection to the aspirated
position could also occur but there would not be an
impermeable torus to seal the pit opening.
2.1. Induction of a critical size gas bubble
The beginning of an embolisation process, where a water
conduit in the xylem is eventually lled with air, is the
induction of a gas bubble past the critical size by actual
phase transition through heterogeneous nucleation, but
more likely by air-seeding from an adjacent lumen or a
crack in the conduit wall (e.g. Tyree, 1997). The reader can
turn to e.g. Tyree (1997) and Steudle (2001) for more
details about these processes. For the modeling presented
here, the actual mechanism responsible for the past critical
size bubble formation does not effect the results. The
general term cavitation will be used in this study to refer to
all of the above processes as this is customary, although
only heterogeneous nucleation can be considered cavitation
in the strictest physical sense (Holtta et al., 2002). The
radius of the critical size bubble is determined by the
pressure difference between the liquid and gas phase, and
surface tension of water according to the Laplace equation
(Brennen, 1995):
RC

Fig. 1. (A) Expanding spherical gas bubble in water conduit with

torusmargo type pits. The pits are un-aspirated in the beginning of the
growth process, as the water pressure in the conduit hosting the bubble has
not yet risen high enough. Water ows out of all the pits connecting the
embolising conduit to adjacent conduits. (B) Expanding spherical gas
bubble in water conduit. The pits have become aspirated as the pressure
difference between the conduit hosting the bubble and adjacent conduits
has risen above a threshold value. (C) Spreading of the gas phase in a
water conduit treated as a capillary. The pits remain aspirated, as the
pressure difference between the conduit hosting the bubble and adjacent
conduits has risen. Water ows out only from the conduit wall area that is
covered with water.

pits still remain un-aspirated. In Fig. 1B the bubble radius

has grown and the bubble is still spherical. The pit
membranes have been displaced to the sides of the adjacent
conduits under tension (i.e. the pits are aspirated) due
to the water pressure difference between the conduits.

2g
,
Pg  Pl

(1)

where RC is the radius of the critical size bubble, g is the

surface tension of water, Pg and Pl are the gas and liquid
phase pressures. The radius RC is the same as the radius of
a maximum pore size in the pit membrane needed to cause
air seeding.
2.2. Dynamics of a bubble past the critical size in the initial
phase where the bubble is spherical
The dynamics of a spherical bubble, in the absence of
thermal effects and incompressible liquid, can be described
by the RayleighPlesset equation (e.g. Brennen,1995):
 
d2 R 3 dR 2 Pg  Pl 4m dR
2g
R 2

,
(2)


dt
2 dt
R dt rL R
rL
where R is the bubble radius, t is time, Pg is the gas pressure
inside the bubble, Pl is the water pressure inside the lumen
hosting the bubble, rL is water density, m is the dynamic
viscosity of water, and g is the surface tension of water.
The gas pressure inside the bubble (Pg) will always have a
value between saturation vapor pressure and atmospheric

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114

pressure, depending on the rate of air diffusion from the

water into the bubble. Air diffusion between the gas and
water is not modeled here, and the gas pressure inside the
bubble Pg will be given a constant value of saturation
vapor pressure, i.e. air diffusion is considered to be slow
compared to the time scale of the process.
The change in water pressure in the conduit hosting the
bubble due to changes in conduit volume is calculated from
Hookes law (e.g. Dainty, 1963).
dPl
1
dV
Er
V
dt
dt

(3)

where Er is the volumetric elastic modulus of the conduit, V

is the conduit volume, and dV is the change in the conduit
volume. Two processes affect the change in conduit
volume: the change in gas bubble volume as bubble radius
changes and the exchange of water with adjacent xylem
conduits. dV is explicitly written
dV
dR
4pR2
 kPl  P0
dt
dt

(4)

where P0 is the water pressure of the adjacent conduits, and

k is the hydraulic conductance (m3 Pa1 s1) of the xylem
conduit. The rst term on the right-hand side of Eq. (4)
equals the volumetric growth of the bubble and the second
term is the water ow from the conduit hosting the bubble
to adjacent conduits. The water pressure inside the
adjacent conduits, P0, does not remain constant, but varies
as the water pushed from an embolising conduit will affect
the water balance of the adjacent conduits.
2.3. Growth of the gas phase after it has contacted lumen
walls
Eqs. (2)(4) describe bubble dynamics when the bubble
is small enough to remain spherical. However, when the
bubble radius reaches the radius of the conduit, the gas
bubble cannot be considered a spherical bubble any
more. Instead, the growth of the gas phase is now described
as spreading of a gas phase in a capillary, where the
pressure exerted by the gas phase pushes water out of
the conduit. Capillary analogy is used because the length of
the conduit is very large compared to its diameter. We
make an assumption that the gas bubble is initially in the
middle of the conduit. The spreading of the gas phase in
the conduit may now be obtained from the Hagen
Poiseuille equation
dl g pr4cond

DP,
dt
8ml g

(5)

where lg is the distance of gas/liquid interface from the

center of the conduit, and DP is the pressure difference
between the liquid and gas phase in the conduit, and rcond is
the conduit radius. This pressure difference DP is written
DP Pg  Pl 

2g cos a
,
rcond

(6)

where is a is the contact angle between the liquid phase

and the conduit wall. The last term on the right-hand
side of the equation is the capillary pressure, and it is
resisting the spreading of the gas phase. Here we assume
the conduit wall to be totally wettable, i.e. a is set to zero.
Eq. (3) is now again used to calculate the relation between
the water pressure and conduit volume. The term dV
is now written
dV
dl g
pr2cond
 kPl  P0 Cl g
(7)
dt
dt
where rcond is the conduit radius, and variable C, which is
dependent on lg, is introduced to be the fraction of the total
conduit wall area, which is covered with water. C is added
as water can only ow out of the conduit at locations where
there is hydraulic connection with the conduit wall. Again
the rst term on the right-hand side of Eq. (7) equals the
volumetric growth of the bubble and the second term is the
water ow from the conduit hosting the bubble to adjacent
conduits.
2.4. Calculation of the hydraulic resistance between the
conduit hosting the bubble and adjacent conduits
The hydraulic conductance k between the conduit
hosting the bubble and the adjacent conduits is calculated
from the conductance the pits and the cell wall connected
in parallel.
k kp N pits kcw

(8)

where kp is the hydraulic conductance of one pit, kcw is the

conductance of the cell wall, and Npits is the number of pits
in the conduit (connected in parallel). The conductance of
the cell wall will be important only if the pits are aspirated
as un-aspirated pits provide a parallel pathway with much
lower resistance.
Pit conductance is constant for angiosperm pits as there
is no impermeable torus which position determines the
resistance to water ow. In theory, the pit conductance of
angiosperm type pits should increase slightly when
subjected to a pressure difference over it as the pit
membrane and the pores will stretch (Sperry and Hacke,
2004), but this is not taken into account here. For
gymnosperm pits with a torusmargo structure the situation is different. The conductance of a gymnosperm pit can
vary from that of an un-aspirated pit where the torus is in
the middle of the pit chamber to zero in a fully aspirated
state. The position of the torus and the conductance to ow
is dependent on the force acting on the pit membrane and
the structure and rigidity of the pit membrane. Following
the protocol of Bolton and Petty (1978), the conductance
of a gymnosperm pit can be broken down into several
conductances in series: that of the pit apertures, the pores
in the margo, and the border-torus annulus. The gymnosperm pit and its components are depicted in Fig. 2A. The
parameters used to describe the geometry of the pit are
presented in Fig. 2B. The pit aperture conductance ka is

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T. Holtta et al. / Journal of Theoretical Biology 249 (2007) 111123

115

Fig. 2. (A) A schematic illustration of a gymnosperm pit with a torusmargo structure. Symbols: (1) pit aperture, (2) pores in the margo and (3) bordertorus annuli. (B) The parameters used to describe the geometry of the pit.

calculated from the HagenPoiseuille equation

4

ka

pK
8LK Z

(9)

where LK and K are the length and radius of the aperture

(see Fig. 2). The conductance of the pit membrane pores km
in the margo is calculated from the HagenPoiseuille
equation between water ow and pressure difference
km

8prpore 4 npore
l pore 1:15rp Z

(10)

where rpore is the pore radius, npore is the number of pores

and lpore is the length of a pore, which is the same as the
margo thickness.
The conductance of pit apertures and pit membrane
pores will be constant even when the pit membrane is
deected. The conductance of the border-torus annulus will
change according to the distance of the torus from the pit
opening H. The conductance of the border-torus annuli is
calculated to be the ow rate divided by the pressure drop
over border-torus annuli from the following equation
(Bolton and Petty, 1978):

 "
 2 #
3QZ lnM=K
Q 2
K
P
0:771r
2
(11)
4pKH
M
4pH 3
where Q is the water ow rate, M is the torus radius.
H decreases as the membrane is deected. When H goes to
zero the, pit becomes fully aspirated and no water will ow
through the pit. The rst term on the right-hand side is the
HagenPoiseuille equation modied for the geometry of
the situation, while the second term gives the kinetic energy
correction. The kinetic energy correction is needed when
the velocity of water ow will be very high. This will occur

when the pit is near to aspiration but mass ow through the

pit still remains high.
Pit membrane deection is calculated from the force
acting pit membrane. In equilibrium, the force acting on
the membrane is balanced by the tension in the margo
strands holding the pit membrane in place. Therefore the
density, width and elastic modulus of the margo strands
holding the pit membrane in place, and the height and
width of the pit chamber need to be known (e.g. Hacke
et al., 2004; Bolton and Petty, 1978; Gregory and Petty,
1973, 1972). The force acting on pit membrane is the
pressure difference created by the ow over the pit
membrane pores and border-torus annulus, i.e. the
pressure drop calculated from Eqs. (10) and (11), times
the cross-sectional area of the torus (Bolton and Petty,
1978). In case of no ow through the pits, i.e. when the pits
are aspirated, the force acting on the pit membrane is the
hydrostatic pressure difference between adjacent conduits
times the cross-sectional area of the torus. The formula
describing the relationship between the pressure difference
over the pit membrane and pit membrane deection is
(Petty, 1972)
DPp

 2
Dm
ns Eer Af siny,
2

(12)

where DP is the pressure difference over the membrane, Dm

is the torus diameter, ns is the number of margo strands,
E is the strain of the margo strands, er is the elastic
modulus of the strands, Af is the cross-sectional area of the
strands, and y is the angle of deection of the pit
membrane from the middle of the pit chamber. By taking
geometrical considerations into account, the pressure
difference from Eq. (12) can be expressed as a solely as

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116

the function of H (Petty, 1972)

0q
1


2
4ns er Af @ LM B  H
B  H
A
DP
1
,
LM
LM
pD2m

xylem pressure Pbulk. Equation for mass conservation is

(13)

where LM is the margo strand length. The total conductance of a gymnosperm pit is calculated to be the
conductances of the three different components used to
describe the pit (Eqs. (9)(11)) connected in series. The pit
aperture and border-torus annuli conductance are calculated twice, as there are two pit apertures and border-torus
annuli for the ow to cross. For the border-torus annuli,
the value of H is different for the upstream and downstream components. For calculating the relation between
the water ux and pressure difference in the upstream
border-torus annulus, the last term in brackets is substituted by its reciprocal (Bolton and Petty, 1978).
2.5. Modeling the change in water balance of adjacent
conduits as a result of water freed from the embolising
conduit
Water freed from an embolising conduit will affect the
water content and water pressure of the conduits surrounding embolising conduit (the term P0 in Eqs. (4) and (7)). As
water is freed from the embolising conduit, it is pushed
to adjacent conduits, and their water pressure will rise
because of this. This rise in water pressure will in turn
induce water ow further away from the embolising
conduit. To estimate this effect on the embolism process,
the transient water and pressure balances of conduits
directly adjacent to the embolising one and conduits
which are at most N conduits distance away from the
embolising conduit are also modeled. N is given the
value 100. Increasing N beyond this does not have any
noticeable effects on the results. The embolising conduit is
assumed to be in direct hydraulic contact with M adjacent
conduits.
Water inow to conduit i 1 equals one Mth of the
water ow from the embolising conduit
kPl  P1 Cl g
i 1,
(14)
M
where Qi,in is the inow rate to conduit i and Pi is the water
pressure in conduit i, and M is the number of neighboring
conduits. Water inow Qi;in to conduits i 41 is

Q1;in

Qi;in kPi  Pi1 i41.

(15)

Water ow out of the conduit i (Qi,out) is equal to the

inow to conduit i+1 for ioN
Qi;out Qi1;in

(16)

ioN

and
QN;out kPN  Pbulk

i N

(17)

for i N. This means that water from the conduit N is

connected to an innite water volume reservoir with bulk

dmi
Qi;in  Qi;out ,
(18)
dt
where mi is the mass of water in conduit i. The consequent
pressure changes are calculated from Hookes law
dPi
1 dmi
Er
,
rV dt
dt

(19)

where r is the density of water. Here we do not consider the

effects of other xylem tissue such as bers and living cells
surrounding the embolised conduit. Tissue with elasticity
such as living cells would be expected to show less change
in pressure when its water content varies. For gymnosperm
wood the fraction of other tissue in the xylem is typically
small and the effect of the capacitive tissue would be low.
2.6. Solving the equations
The independent variables R, Pl, V, and P0 in Eqs. (2)(4),
and (19) for the spherical bubble, or alternatively the
independent variables lg, Pl, V, and P0 in Eqs. (3), (5), (7),
and (19) for the gas spreading in a capillary, are coupled
non-linear differential equations which are solved numerically. Initial values are given to them and then their time
development is solved using the fourth-order RungeKutta
method (Press et al., 1989) for the spherical bubble case and
Euler method for the capillary case. The value of the time
step is chosen so that changing that value does not have any
noticeable inuence on the results. The time step used has to
be very small, especially in the beginning of the process. For
gymnosperms with torusmargo type pits, the transient
torus displacement and pit conductance are solved iteratively during each time step by nding the correct torus
displacement simultaneously while the pressure difference
over the torus is solved.
3. Parametrization
Parameters used in the base case model simulations are
listed in Table 1. The values for the base case have been
chosen to represent a typical gymnosperm earlywood
tracheid with a torusmargo structure and a typical
angiosperm vessel. The bulk xylem water pressure is given
a value 1.0 MPa, a typical value during transpiration.
This is the initial value for the water pressure in the
embolising conduit and in the adjacent conduits. The
radius and length of a gymnosperm conduit are given
values of 20 mm and 3 mm, respectively. These are typical
values for earlywood gymnosperm tracheids (Lancashire
and Ennos, 2002). The values given for angiosperm vessel
radius and length are 50 mm and 3 mm, respectively. The
initial value for the bubble radius is calculated from Eq. (1)
to be 1.46  107 m. The elastic modulus of the conduit is
given a value 750 MPa (Peramaki et al., 2001). Saturation
vapor pressure was given the value 0.003 MPa, and surface
tension of water is given the value 0.073 N m1. These

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T. Holtta et al. / Journal of Theoretical Biology 249 (2007) 111123
Table 1
Parameters used in the model

Table 2
Parameters used for detailed description of gymnosperm pits, values are
from Bolton and Petty (1978)

Initial xylem pressure

(Pl)

1.0 MPa

Hydraulic conductance
of the cell wall (kcw)
Gymnosperm conduit
radius (rcond)
Gymnosperm conduit
length (l)
Number of pits in a
gymnosperm conduit
(Npits)
Angiosperm conduit
radius (rcond)
Angiosperm conduit
length (l)
Angiosperm pit
conductance (kp)
Number of pits in a
angiosperm conduit
(Npits)
Conduit elastic modulus
(Er)

8  1021 m3 Pa1 s1

Estimated

20 mm

100

Lancashire and
Ennos (2002)
Lancashire and
Ennos (2002)
Usta (2005)

50 mm

Estimated

3 mm

Estimated

1.67  1017 m3 Pa1 s1

Estimated

250

Estimated

750 MPa

Peramaki et al.
(2001)

3 mm

117

Estimated

values are for water at 25 1C. The number of pits in a

gymnosperm conduit is estimated to be 100. According to
Usta (2005), the number of pits per earlywood tracheids
varies from 50 to 300. The number of pits in an angiosperm
conduit is calculated from the gymnosperm value, assuming the pit density per cell wall area is the same for both, to
be 250. The dimensions, surface area, elasticity, and
hydraulic conductivity of the conduits adjacent to the
embolising conduit are made equal to that of the
embolising conduit. The number of conduits connected to
the embolising conduit M is given a value of 4.
The cell wall conductance was given a value
8  1021 m3 Pa1 s1. Only a few studies have been made
about the hydraulic conductance through the xylem conduit
cell wall (De Boer and Volkov, 2003). Wisniewski et al.
(1987a, b) found that the primary and secondary walls of
vessel elements of various woody plant species, except parts
that were associated with the pit membranes, were impermeable to lanthanum nitrate, which can penetrate capillaries as
small as 2 nm. This suggests that the cell walls have a very
low permeability to water (De Boer and Volkov, 2003).
Petty and Palin (1981, 1983) measured the tangential and
radial cell wall permeability of tracheids of the order of
10211020 m2. Assuming a cell wall thickness of 6 mm and
viscosity of pure water at 25 1C, this value can be converted
into conductance, and is found to be over ten times larger
than our value. However, the method they used most likely
overestimates the permeability (Aumann and Ford, 2002).
Aumann and Ford (2002) used a value of 2.25  1019 m s1
for cell wall conductivity of tracheids. Assuming a cell wall
thickness of 6 mm, this value can be converted into
conductance, and is found to be approximately one
thousandth of our value. No values for the conductance of

Cross-sectional area of micro-bril strands (Af)

Number of micro-bril strands in margo (ns)
Elastic modulus of strands (er)
Maximum torus displacement (B)
Pit membrane diameter (Dm)
Torus radius (M)
Margo strand length (LM)
Pit aperture radius (K)
Pit aperture length (LK)
Number of pores in margo (npore)
Margo pore radius (rpore)
Margo pore thickness (lpore)

707  1018 m2
100
3 Gpa
2  106 m
17.0  106 m
4.25  106 m
4.25  106 m
2.7  106 m
1.5  106 m
200
2.1  107 m
1.5  107 m

the aspirated pits were found in the literature, although it is

stated in many references that the torus is impermeable to
water (e.g. Gregory and Petty, 1973; Pittermann et al.,
2005). Therefore, the conductance of aspirated pits is
assumed to be the same as that of the cell wall.
Table 2 shows the parameters used for the gymnosperm
torusmargo type pit structure. Although there are many
individual parameters in Table 2 describing pit structure
and its elastic behavior, more important than the values of
these individual parameters is their combined effect on pit
conductivity and the force required for complete pit
aspiration. Eqs. (911) and parameters in Table 2 for the
description of a gymnosperm pit yield a value of
1  1015 m3 Pa1 s1 for the conductance of single
un-aspirated pit. This is similar to values reported in the
literature (e.g. Lancashire and Ennos, 2002). An angiosperm pit with a homogeneous pit membrane was given a
conductance one-sixtieth of this (Pittermann et al., 2005).
Similarly, the parameters give a pressure difference of
0.19 MPa required to aspirate the pit, which is in
accordance with pressure differences calculated for pit
aspiration for gymnosperms by Bolton and Petty (1978)
and Hacke et al. (2004). An initial time step of 1012 s was
used, from where it is gradually raised to 108 s. Running
our numerical model on a fast Unix computer allowed us
to use such a small time step. With a larger time step, the
numerical solution would become unstable.
In the Results section we demonstrate the dynamics of
embolism growth for a typical gymnosperm pit with a
torusmargo structure and a typical angiosperm conduit
with a homogeneous pit membrane using the model
presented above. Also sensitivity analysis to the most
important parameters affecting embolism formation
dynamics is done.
4. Results
4.1. Gymnosperms with a torusmargo pit structure
The dynamics of the bubble and the gas phase growth
for the base case parameterization with a gymnosperm

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T. Holtta et al. / Journal of Theoretical Biology 249 (2007) 111123

Fig. 3. (A) Bubble radius (gray line) and torus displacement H (dark line) as a function of time for the base case parameters for a gymnosperm conduit
with torusmargo pit structure. Time is calculated from the induction of a critical size bubble. The arrow marks pit aspiration. (B) Water pressure in the
conduit (gray line) and the adjacent conduits (dark line). (C) Water ux out of the embolising conduit (dark line) and hydraulic conductance of the conduit
(gray line). (D) Relative volume of water in the conduit hosting the embolism as a function of time.

torusmargo structure is demonstrated in Fig. 3. Time is

calculated from the induction of the critical size bubble.
Initially the bubble radius (Fig. 3A) grows rapidly as the
pressure difference between the bubble (saturation
vapor pressure) and the liquid water in the water conduit
(Fig. 3B) is large and the pit is un-aspirated. As the water
pressure in the embolising conduit rises more rapidly than
in the adjacent conduits water ux between the embolising
conduit and the adjacent conduits (Fig. 3C) increases. The
pit membrane displacement (Fig. 3A) increases as the force
deecting it grows until the value required for pit
aspiration is reached and the pit becomes shut as it
aspirates. The force acting on the torus (inset Fig. 3B) is
almost equal to the pressure difference between the
embolising and adjacent conduits. The moment of pit
aspiration is shown with an arrow. Following aspiration,
hydraulic conductance to water ow out of the conduit
decreases by many orders of magnitude (Fig. 3C) and
growth of the bubble slows dramatically. After reaching
the conduit diameter, at approximately 3 s, the gas phase
spreads in the capillary (Fig. 3D). The water pressure in
the conduit in the capillary phase (Fig. 3B) remains nearly
constant. The pressure is dictated by the gas phase and the
capillary pressures. As the water pressure in the adjacent
conduit (Fig. 3B) remains essentially constant during the
whole process, the driving force for the water ow out of
the conduit remains almost constant in the capillary phase.

The pits remain aspirated as there is a hydrostatic pressure

difference over the torus which remains higher than
threshold for pit aspiration. The water ow rate out of
the conduit decreases gradually as the gas spreads because
the fraction of the conduit wall covered with water
decreases (Fig. 3D). Full embolism is achieved in about
20 min. The Reynolds number, estimated from the equation for water ow through a pipe, reaches a maximum
value of approximately 10 in the border pit annuli of the
pits just before the pits aspirate (not shown), and then
drops abruptly. The ow is therefore likely to remain
laminar at all times. If turbulence would arise it would be
minor and occur just prior to pit aspiration, and it would
not have signicant effect on the results.
4.2. Angiosperms with a homogeneous pit structure
The dynamics of embolism growth is very different for a
conduit with a homogeneous angiosperm pit. Initially, the
bubble radius (Fig. 4A) has the same dynamics as in the
torusmargo case, but continues fast growth unlike in the
previous case as pit conductivity does not drop due to
pit aspiration. Water pressures in the embolising conduit
(Fig. 4B) rises initially very fast, but the pressure rise slows
down as the water pressure in the adjacent conduits
(Fig. 4B) rises much above bulk xylem pressure. The
whole embolisation process is now much faster (Fig. 4C),

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119

Fig. 4. (A) Bubble radius as a function of time for the base case parameters for an angiosperm conduit with a homogeneous pit structure. (B) Water
pressure in the conduit (gray line) and the adjacent conduits (dark line). (C) Relative volume of water in the conduit hosting the embolism as a function of
time.

occurring in a fraction of a second. Similar dynamics

would be expected for a pit with a torusmargo structure if
the pits would not aspirate. Although embolism formation
is rapid, it is actually slow compared to bubble growth in
bulk water under the same tension. The time needed for a
bubble to grow to the same volume as the base case xylem
conduit in bulk water under the same tension can be
calculated from Eq. (2) to be approximately 50 ms.
4.3. Sensitivity for parameters
The time required for the bubble to ll the conduit
completely as a function of the bulk xylem water pressure
for the conduit with a torusmargo structure, i.e. the case
presented in Fig. 3, is illustrated in Fig. 5. The time needed
for complete embolism has a maximum at a xylem pressure
where the developing water pressure difference between the
embolising and adjacent conduits reaches the threshold for
pit aspiration. The xylem water pressure at the maximum
embolism time is about 0.2 MPa in this case. At xylem
pressures higher than this, i.e. at lower water tensions, the
pits will not aspirate and embolism is fast. At lower xylem
pressures than the one which causes the maximum in
embolism time, the time needed for complete embolism
increases as the bulk xylem water pressure decreases
because then the pressure difference driving water out of
the conduit is larger. In the case of a homogeneous pit

membrane (not shown), embolism time always increases

with increasing xylem pressure, i.e. with decreasing xylem
tension.
For a case with a torusmargo structure, i.e. the case
presented in Fig. 3, the cell wall conductance will determine
the resistance of water ow out of the embolising conduit
after aspiration has occurred and will therefore inuence
embolism time strongly (Fig. 6A). Embolism time is
inversely proportional to the hydraulic conductance of
the cell wall. Varying the hydraulic conductance of the pits
did not affect the base case results very strongly. Lowering
pit conductance did not have practically any effect on the
results. With increased pit conductance, the total embolism
time will be slightly shorter as it takes longer for pits to
aspirate (Fig. 6B). For the homogeneous angiosperm pits
cell wall conductance does not affect embolism dynamics,
as long it remains much lower than the conductance of the
pits. A lower pit hydraulic conductance will result in an
increase in the embolism time and a higher conductance
will decrease it (Fig. 6C). The decrease in embolism time
will become less pronounced as the conductance grows to
very high as then pressure distribution in the adjacent
conduits is also affected strongly.
The effect of various other parameter values on the
embolism dynamics was also tested. For conduits with
torusmargo type pits, decreasing the elasticity of the pits,
for example by increasing the elastic modulus of the margo

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T. Holtta et al. / Journal of Theoretical Biology 249 (2007) 111123

Fig. 5. Time needed for complete embolism as a function of the xylem water pressure for a gymnosperm conduit with torusmargo pit structure.

Fig. 6. (A) Time needed for complete embolism as a function of the cell wall conductance for a gymnosperm conduit with torusmargo pit structure.
Values in the x-axis are shown relative to the base case values. (B) Time needed for complete embolism as a function of the pit conductance for a
gymnosperm conduit with torusmargo pit structure. (C) Time needed for complete embolism as a function of the pit conductance for an angiosperm
conduit with a homogeneous pit structure.

strands, would increase the threshold pressure for pit

aspiration linearly. Less elastic pit membranes would need
higher bulk xylem tensions for pit aspiration. If pit density
is constant, wider conduits will take longer to embolise as
they have a larger volume to surface area ratio than
narrower conduits, i.e. more water has to ow out through
relatively a smaller conduit wall area. The relationship

between conduit diameter and embolism time is linear.

Conduit length was found not to have any affect on
embolism time, as the conduit volume to conduit wall area
ratio remains constant with varying conduit length. If the
number of functioning water conduits directly adjacent to
the embolising one were reduced along with surface area
which the embolising conduit could exchange water with

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T. Holtta et al. / Journal of Theoretical Biology 249 (2007) 111123

adjacent conduits, then embolism time increased by

approximately the same factor as the neighboring conduits
and surface area were reduced. Changing the elastic
modulus did not practically affect the growth rate, as long
as it was not reduced to magnitudes much below reasonable. The past critical size bubbles were not found to
collapse in any situation as the conduit water pressure does
not rise higher than the gas pressure at any time during the
bubble growth process. Sub-critical size bubbles always
collapsed. These results are not shown in the gures.
5. Discussion
The principle aim of this study was to model the timescale required for the gas phase induced by cavitation to ll
an entire xylem conduit, i.e. to fully embolise a conduit.
Embolism formation was found to be slower from what
would be expected for a bubble to grow in bulk water.
While gas bubbles would grow very rapidly in bulk water
under tension, the inelasticity of the conduit walls together
with hydraulic resistance of the conduit lumen and
bordered pits will restrain the gas phase growth. As the
conduit cannot expand much when the gas phase volume is
growing, ow rate of water out of the conduit in turn is
determined by the developing pressure difference between
the embolising and adjacent conduit and the hydraulic
conductance of the water conduit. Although transpiration
is not explicitly present in the model, transpiration rate will
determine the xylem bulk water tension, and therefore the
pull which drains water out of the embolising conduit. For
torusmargo type gymnosperm pits, the time-scale of
the process was found to be strongly dependent on the
functioning of the bordered pits between conduits. If the
force exerted by the water ow out of the embolising
conduit on the pit membrane grows larger than the force
needed to aspirate the pits, embolism formation will
become much slower, as water from the conduit will be
slowly drained through the cell wall. The time needed for
complete embolism will then be determined by the
conductance of the cell wall, bulk xylem pressure, and
conduit radius. The force per unit area acting on the torus
was found to be nearly as large as the difference in water
pressure between the embolising and adjacent conduits.
This is because almost the entire pressure drop on the
pathway between the embolising and adjacent conduits
occurs at the margo pits (when the ow rate is small) or the
border-torus annuli (when the ow rate is large) where it is
applicable to displace the torus. Unlike gymnosperm
earlywood tracheids, latewood tracheids would not be
expected to aspirate at the water uxes and water pressure
differences caused by embolism as their structure and
rigidity will resist aspiration up to much higher pressure
differences (e.g. Petty, 1972; Siau, 1984).
The water pressure in the conduit hosting the bubble was
found to reach its saturation value, i.e. a value where the
water pressure is the sum of pressure of the gas phase and
the capillary pressure, already in the very beginning of the

121

embolism process in the base case. This happens as the

water cannot ow out of the embolising conduit at
the same volumetric rate as the gas phase expands, so
water pressure in the conduit rises by many atmospheres in
as little as few microseconds. The rapid tension release is
also transmitted to the conduit walls, and this is probably
the signal that is observed in acoustic and ultra-acoustic
monitoring of cavitation events (e.g. Tyree and Dixon,
1983). Water pressure in the adjacent conduits remained
close to bulk xylem water pressure after pit aspiration
occurred. In this case the driving pressure difference
for water ow out of the conduit could be approximated
quite accurately to be the difference between saturation
vapor pressure and bulk xylem pressure. However, this
was shown not to be the case in the absence of pit
aspiration, where water is emptied very fast out of the
embolising conduit, and water pressure in the surrounding
conduits can rise noticeably and affect the embolism
dynamics. The water released from the embolising conduit
and the consequent rise in water pressure of the adjacent
conduits could also have a capacitive role during times of
water decit (e.g Meinzer et al., 2001). This water freed
from the embolising conduit to the adjacent tissue will
supply extra water, and might prevent the bulk water
potential from falling to harmfully low levels during peak
water stress.
Of the various parameters, the hydraulic conductance of
the conduit when the pits are aspirated, which practically
reduces to being the hydraulic conductance of the cell wall,
is probably the least well-known of the various parameters
(De Boer and Volkov, 2003; Aumann and Ford, 2002), and
will affect the total embolism time very dramatically in the
case of pit aspiration for conduits with torusmargo type
pits. Therefore the times predicted here for complete
embolism in this case are not meant to be accurate, even
to the order of magnitude. If we calculate the total
embolism time from the two extreme cell wall conductance
values given in the literature, the high value given by Petty
and Pallin (1981, 1983) and the low value from Aumann
and Ford (2002), the time scale for complete water
drainage out of a conifer conduit with aspirated pits could
range from tens of seconds to an approximately a month if
other parameters were to be as in the base case. However, if
even one of the pits would remain un-aspirated, for
example due to a more rigid structure, then this one pit
would provide a much lower resistance pathway out of the
embolising conduit, and the time-scale for embolism
formation would be comparable to the homogeneous pit
membrane case.
The dynamics described here for embolism formation are
for a case where a single conduit is embolising surrounded
by other water conducting conduits connetected to the
transpiration stream. If also other conduits were to
embolise during the time-scale described here, this would
raise the water pressure in the adjacent conduits due to
water release from the other embolising conduits. Theoretically, this would decrease water ux out of the embolising

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conduit and therefore decrease the likelihood of pit

aspiration and slow down embolism formation in other
cases. Whether the gas inside the bubble has atmospheric
pressure, i.e. air is assumed to diffuse very fast to the
bubble, or saturation vapor pressure, i.e. no air diffusion,
has only a small effect on the bubble growth rate. Air lled
gas phase grows slightly faster than a water vapor lled
because the pressure gradient driving water out of the
conduit is approximately 0.1 MPa larger in the air lled
case. Our model might slightly overestimate the growth
rate of gas phase because the whole conduit area covered
by liquid water is taken as the area that can exchange water
with adjacent conduits in the model. If a part of this area
would not be able to exchange water, then water ow out
of the embolising conduit would also be slower. Also the
tapered ends of the conduits are not formulated in the
model. The capillary pressure resisting the bubble growth
would actually increase at the nal stages of the embolism
process, as the capillary pressure is inversely proportional
to the conduit radius. The tapered ends of the conduit
would thus slightly hinder the spreading of the gas phase.
For the torusmargo type pits, the long time possibly
required for complete embolism formation might have
consequences on the ability to rell embolised conduits.
Possibly relling could commence before all of the water is
drained out of the conduit. Hydraulic isolation from
adjacent conduits has been proposed to be a requisite for
complete embolism relling of a conduit (Holbrook and
Zwieniecki, 1999). Zwieniecki and Holbrook (2000) show
that this could be accomplished by the air spaces in the pits
which would be dissolved only at very end of the relling
process and hydraulic contact would then be re-achieved.
Hydraulic isolation would also occur between the embolising conduit and adjacent conduits as a result of the pit
aspiration modeled in this study.
Acknowledgement
Helsingin Sanomain 100-vuotissaatio is acknowledged
for the research funding.
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