Water deficits and hydraulic limits to leaf water supply


Sperry, J.; Hacke, U.; Oren, R.C.mstock, J.

Plant cell and environment 25(2): 251-263

2002


Many aspects of plant water use--particularly in response to soil drought--may have as their basis the alteration of hydraulic conductance from soil to canopy. The regulation of plant water potential by stomatal control and leaf area adjustment may be necessary to maximize water uptake on the one hand, while avoiding loss of hydraulic contact with the soil water on the other. Modelling the changes in hydraulic conductance with pressure gradients in the continuum allows the prediction of water use as a function of soil environment and plant architectural and xylem traits. Large differences in water use between species can be attributed in part to differences in their 'hydraulic equipment' that is presumably optimized for drawing water from a particular temporal and spatial niche in the soil environment. A number of studies have identified hydraulic limits as the cause of partial or complete foliar dieback in response to drought. The interactions between root:shoot ratio, rooting depth, xylem properties, and soil properties in influencing the limits to canopy water supply can be used to predict which combinations should optimize water use in a given circumstance. The hydraulic approach can improve our understanding of the coupling of canopy processes to soil environment, and the adaptive significance of stomatal behaviour.

Plant,
Cell
and
Environment
(2002)
25,251-263
Water
deficits
and
hydraulic
limits
to
leaf
water
supply
J.
S.
SPERRY,
1
U.
G.
HACKE,
1
R.
OREN
2
&
J.
P.
COMSTOCK
3
1
Department
of
Biology,
University
of
Utah,
Salt
Lake
City,
UT,
84112,
USA,
2
Nicholas
School
of
Environment,
Duke
University,
Durham,
NC,
27708,
USA
and
3
Boyce
Thompson
Institute
for
Plant
Research,
Tower
Road,
Ithaca,
NY,
14853,
USA
ABSTRACT
Many
aspects
of
plant
water
use
particularly
in
response
to
soil
drought
may
have
as
their
basis
the
alteration
of
hydraulic
conductance
from
soil
to
canopy.
The
regulation
of
plant
water
potential
(W)
by
stomatal
control
and
leaf
area
adjustment
may
be
necessary
to
maximize
water
uptake
on
the
one
hand,
while
avoiding
loss
of
hydraulic
contact
with
the
soil
water
on
the
other.
Modelling
the
changes
in
hydraulic
conductance
with
pressure
gradients
in
the
continuum
allows
the
prediction
of
water
use
as
a
function
of
soil
environment
and
plant
architectural
and
xylem
traits.
Large
differences
in
water
use
between
species
can
be
attributed
in
part
to
differences
in
their
'hydraulic
equipment'
that
is
presumably
optimized
for
drawing
water
from
a
particular
temporal
and
spatial
niche
in
the
soil
envi-
ronment.
A
number
of
studies
have
identified
hydraulic
limits
as
the
cause
of
partial
or
complete
foliar
dieback
in
response
to
drought.
The
interactions
between
root:shoot
ratio,
rooting
depth,
xylem
properties,
and
soil
properties
in
influencing
the
limits
to
canopy
water
supply
can
be
used
to
predict
which
combinations
should
optimize
water
use
in
a
given
circumstance.
The
hydraulic
approach
can
improve
our
understanding
of
the
coupling
of
canopy
processes
to
soil
environment,
and
the
adaptive
significance
of
stomatal
behaviour.
Key-words:
drought
responses;
hydraulic
architecture;
plant—soil
interactions;
stomatal
regulation;
water
relations;
water
transport;
xylem
cavitation.
INTRODUCTION
In
this
review,
we
consider
how
the
stomatal
response
to
water
stress
is
influenced
by
stress-induced
changes
in
the
hydraulic
conductance
of
the
soil—leaf
pathway.
We
evalu-
ate
the
thesis
that
stomatal
regulation
(and
longer-term
leaf
area
regulation)
of
gas
exchange
is
necessary
to
preserve
hydraulic
continuity
of
the
soil—leaf
continuum,
and
that
without
such
regulation,
the
advantages
of
vascular
tissue
and
root
systems
for
mining
soil
water
could
not
be
fully
exploited
(Tyree
&
Sperry
1988;
Jones
&
Sutherland
1991;
Sperry
et
al.
1998;
Sperry
2000).
Correspondence:
J.
S.
Sperry.
Fax:
801
5814668;•
e-mail:
The
function
of
stomata
in
water
relations
(not
consid-
ering
additional
CO
2
and
light
responses)
is
like
a
pressure
regulator.
A
pressure
regulator
limits
pressure
changes
by
controlling
flow
rate,
and
the
stomata
limit
the
variation
in
plant
water
potential
(Y')
with
soil
moisture
and
evapora-
tive
demand
by
controlling
transpiration.
In
this
way,
the
plant
avoids
damaging
drops
in
V!
To
function
as
a
pressure
regulator,
the
stomata
must
be
capable
of
sensing
or
pre-
dicting
plant
V'
as
it
changes
with
conditions.
Fortunately,
the
details
of
the
sensing
process
(which
are
the
subject
of
much
investigation;
Jones
1998;
Nardini
&
Salleo
2000)
are
of
no
direct
concern
to
our
topic.
What
is
important
is
the
fact
that
some
form
of
V'
regulation
exists.
It
is
also
not
implied
that
the
regulation
of
V'
need
be
perfect,
or
`isohy-
dric',
only
that
if
plant
V'
does
drop
in
response
to
drought,
as
in
anisohydric
species,
the
drop
is
regulated.
Given
the
pressure
regulator
mode
of
stomatal
function,
it
is
inevitable
that
changes
in
hydraulic
conductance
of
the
soil—leaf
pathway,
soil
moisture,
and
evaporative
demand
will
indirectly
drive
changes
in
stomatal
conductance
and
transpiration
(Saliendra,
Sperry
&
Comstock
1995;
Fuchs
&
Livingston
1996;
Comstock
&
Mencuccini
1998;
Hubbard
et
al.
2001).
Thus,
the
analysis
of
soil—plant
hydraulics
can
be
used
to
explain
and
predict
patterns
of
plant
water
use
with
respect
to
the
soil
and
atmospheric
environment,
and
the
large
differences
between
species
and
cultivars.
This
has
been
a
goal
of
research
on
the
soil—plant—atmosphere
con-
tinuum
(SPAC)
for
over
four
decades
(Gardner
1965;
Philip
1966).
The
earlier
work
tended
to
emphasize
soil
hydraulics,
because
flow
in
the
soil
is
a
physical
process
and
can
be
readily
quantified,
whereas
plant
hydraulics
were
less
well
understood.
Here
we
emphasize
the
important
similarities
between
flow
in
soil
and
flow
in
xylem.
The
incorporation
of
soil
and
xylem
dynamics
can
improve
the
treatment
of
plant
hydraulics
in
SPAC
models
and
set
a
physical
constraint
on
the
stomatal
regulation
of
transpiration
(E)
and
P.
We
begin
with
an
overview
of
the
theoretical
linkage
between
water
transport
and
transpiration.
This
is
followed
by
a
discussion
of
the
behaviour
of
hydraulic
conductivity
along
the
soil—leaf
continuum,
with
an
emphasis
on
the
sim-
ilarity
of
soil
and
xylem
pathways.
A
final
section
considers
examples
of
how
the
hydraulic
approach
has
been
used
to
predict
plant
water
use
and
the
limits
to
gas
exchange.
We
conclude
with
a
discussion
of
the
approach
and
prospects
for
future
research.
For
simplicity,
we
focus
on
the
influence
of
soil
moisture
on
plant
water
use.
A
similar
approach
that
©
2002
Blackwell
Science
Ltd
251
0
0
E
crit
E
PA
mt
meal
0—
--
Drought
(a)
(Negative)
E
(
transp
ira
t
ion
ra
te
p
0
252
J.
S.
Spenyet
al.
emphasizes
the
evaporative
gradient
is
given
in
Oren
et
al.
(1999).
THEORY
If
one
could
make
a
plant
transpire
at
any
rate
E
from
zero
to
infinity
while
holding
the
bulk
soil
water
pressure
con-
stant,
the
trajectory
of
E
versus
leaf
P
(at
steady
state),
could
look
like
Fig.
la.
When
E
is
zero,
the
leaf
P
would
equal
the
bulk
soil
P
(ignoring
gravitational
effects).
As
E
was
increased
there
would
be
a
corresponding
drop
in
leaf
W.
The
E
versus
P
trajectory
will
not
be
a
straight
line
because
the
hydraulic
conductance
of
the
flow
path
will
not
be
constant
with
W.
For
at
least
two
well-understood
rea-
sons,
the
hydraulic
conductance
will
decline
as
P
becomes
lower
with
elevated
E,
creating
a
curved
trajectory
wherein
P
must
drop
disproportionately
with
increasing
E.
These
two
reasons
are
a
loss
of
soil
conductivity
in
the
rhizosphere
between
bulk
soil
and
root
surface
(Newman
1969),
and
cavitation
in
the
xylem
(Tyree
&
Sperry
1989).
Although
there
may
be
additional
changes
in
conductance
with
E,
such
as
variable
aquaporin
activity
in
root
or
leaf
mem-
branes
(Henzler
et
al.
1999;
Clarkson
et
al.
2000),
or
vari-
able
KC1
concentration
in
xylem
sap
(Zwieniecki,
Melcher
&
Holbrook
2001),
the
'P-dependence
of
these
factors
is
not
well
characterized,
as
opposed
to
the
inevitable
physical
processes
of
rhizosphere
drying
and
xylem
cavitation.
The
theoretical
E
versus
W
trajectory
cannot
go
to
infin-
ity,
but
has
a
maximum
steady-state
E-value,
E
ent
(Fig.
la,
solid
line,
open
symbol)
with
an
associated
W
ent
.
Any
higher
steady-state
rate
of
E
is
impossible,
because
the
drop
in
pressure
drives
the
remaining
hydraulic
conductance
in
the
bulk
soil—leaf
pathway
to
zero,
breaking
apart
the
hydraulic
continuum.
The
critical
values
of
E
and
P
describe
a
phys-
ical
boundary
to
gas
exchange
with
respect
to
soil
and
plant
hydraulics.
Transpiration
and
plant
W
must
be
regulated
to
stay
within
these
physical
limits
or
else
canopy
desiccation
will
occur.
The
existence
of
a
hydraulic
limit
means
that
pulling
harder
on
the
water
column
does
not
necessarily
provide
more
water
to
the
leaves.
Oil
workers
are
aware
of
this
con-
cept,
knowing
that
to
extract
the
maximum
oil
volume
from
a
single
well,
pumping
rates
must
be
moderated
to
maintain
fluid
contact
as
flow
resistance
increases
with
fluid
with-
drawal.
Plants
may
need
to
regulate
their
rate
of
water
uptake
to
stay
within
the
hydraulic
limits
of
their
supply
line.
The
E
versus
W
trajectory
can
be
replicated
for
any
bulk
soil
moisture.
A
drier
soil
will
have
a
lower
pressure
inter-
cept
and
a
flatter
E
versus
Wtrajectory
with
a
lower
E
ent
(Fig.
la,
dashed
line,
open
symbol)
than
a
wet
soil
because
the
starting
hydraulic
conductance
(i.e.
at
E
=
0)
is
reduced
under
drier
conditions.
The
drier
the
soil,
the
more
restric-
tive
are
the
hydraulic
limits
to
steady-state
transpiration.
The
curves
in
Fig.
la
are
the
basis
for
predicting
plant
water
use
from
soil
moisture
and
xylem
properties.
If
the
underlying
hydraulic
conductance
changes
are
properly
Leaf
V'
(Bulk
soil
7
1
)
(b)
Water
use
envelope
E
crit
E,
regulation
E,
+
regulation
extraction
Extraction
limit
(—
regulation)
\I(
(Negative)
<
0
Bulk
soil
7'
Figure
1.
Definition
of
hydraulic
limitations
in
the
soil—leaf
hydraulic
continuum.
(a)
Theoretical
steady-state
trajectory
of
transpiration
(E)
versus
leaf
water
potential
(41).
When
E
=
0,
leaf
W
=
W
of
the
bulk
soil.
The
disproportionate
drop
in
leaf
W
with
increasing
E
results
from
the
progressive
W-
induced
loss
of
hydraulic
conductance
in
the
continuum.
The
maximum
permissible
steady-state
E
is
E
crit
:
any
higher
transpiration
rate
drives
the
hydraulic
conductance
to
zero.
E
crit
is
associated
with
corresponding
leaf
W
ait
.
Actual
E
can
be
predicted
(Epred)
from
this
trajectory
from
measured
or
estimated
leaf
7'(W
rneas
).As
bulk
soil
Wbecomes
more
negative
(drought),
the
E
versus
Wtrajectory
flattens
(dashed
curve)
and
hydraulic
limits
become
more
severe.
(b)
The
trajectory
of
E
crit
for
the
soil—leaf
continuum
versus
declining
bulk
soil
(4').
The
E
crit
curve
is
the
plant's
'water
use
envelope'
and
defines
the
upper
boundary
for
steady-state
water
transport
as
a
function
of
soil
W.
The
'extraction
limit'
is
the
bulk
soil
W
at
which
E
crit
becomes
negligible
and
water
cannot
usefully
be
extracted
from
the
soil.
The
extraction
potential
(Fig.
4b)
is
the
area
under
the
envelope.
Shown
also
are
hypothetical
patterns
of
actual
E
with
(+)
and
without
(—)
stomatal
regulation.
Without
regulation
(dotted
line),
once
E
surpasses
E
crit
there
is
no
further
water
uptake,
and
the
ability
of
the
plant
to
extract
water
is
compromised
(extraction,
regulation).
Regulation
of
E
(dashed
line)
is
necessary
for
the
plant
to
stay
within
its
hydraulic
limits
and
fully
exploit
its
potential
for
soil
water
uptake.
characterized,
the
theoretical
curve
will
include
the
actual
E
and
P
of
the
plant
for
steady-state
conditions.
If
there
is
any
information
on
leaf
P
for
steady-state
conditions
either
from
a
direct
midday
measurement,
or
an
assump-
tion
of
isohydric
or
anisohydric
regulation
of
midday
P
(Fig.
la,
V
-
1
„,
eas
)
,
the
midday
E
can
be
predicted
from
the
tra-
jectory
(Epred)
1
,
and
the
safety
margin
from
E
crit
estimated.
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
Water
deficits
and
hydraulic
limits
to
leaf
water
supply
253
The
day-to-day
stomatal
response
to
soil
drought
can
be
predicted
by
calculating
the
E
versus
W
trajectory
for
any
soil
moisture
value,
and
locating
the
plant
on
the
curve
based
on
its
manner
of
W
regulation.
A
convenient
way
of
summarizing
the
prediction
of
water
use
from
soil
and
plant
hydraulics
is
illustrated
in
Fig.
lb.
This
figure
plots
the
and
E
derived
from
individual
curves
like
those
in
Fig.
la
against
the
bulk
soil
P
(=
intercept)
for
each
trajectory.
The
solid
line
in
Fig.
lb
shows
how
E
srit
declines
to
zero
as
soil
moisture
declines.
We
refer
to
this
as
the
'water
use
envelope'
because
it
defines
the
maximum
hydraulically
possible
rate
of
water
use
as
a
func-
tion
of
soil
moisture.
The
minimum
bulk
soil
water
poten-
tial
allowing
any
gas
exchange
is
referred
to
as
the
`extraction
limit',
analogous
in
a
sense
to
the
permanent
wilting
point.
The
thesis
that
stomatal
regulation
is
required
to
pre-
serve
hydraulic
contact
between
soil
and
canopy
and
thereby
maximize
the
soil
water
extraction
by
vascular
plants,
is
illustrated
by
the
dotted
line
in
Fig.
lb
(`-
regula-
tion').
This
shows
what
would
happen
if
there
was
a
con-
stant
midday
stomatal
conductance
as
soil
dried,
assuming
a
constant
evaporative
gradient
and
E.
The
plant
would
reach
E'
en
,
at
a
relatively
high
value
of
bulk
soil
W,
prema-
turely
desiccating
the
canopy.
The
plant's
actual
extraction
in
the
absence
of
any
stomatal
response
(`extraction,
-
reg-
ulation')
would
be
much
less
than
the
hydraulically
defined
extraction
limit.
In
contrast,
the
plant
P
regulation
that
results
from
stomatal
action
(dashed
line,
`-F
regulation')
can
allow
the
plant
to
'push
the
envelope'
while
not
exceed-
ing
it,
thereby
maximizing
gas
exchange
without
interrupt-
ing
water
conduction.
For
the
plant
to
accomplish
this,
the
stomata
must
always
keep
the
midday
Pless
negative
than
Wont
as
soil
moisture
declines.
The
analysis
shown
in
Fig.
1
is
attractive,
because
to
the
extent
it
is
valid,
it
can
be
used
to
explain
and
predict
dif-
ferences
in
maximum
gas
exchange
capacity
and
water
use
between
different
soil
moisture
regimes,
soil
types,
root
sys-
tems,
and
xylem
types.
It
can
be
used
to
predict
plant
traits
that
should
optimize
water
extraction
from
a
particular
soil
environment
for
a
given
investment
in
roots
and
xylem.
However,
to
undertake
such
an
analysis,
the
hydraulic
con-
ductance
in
the
soil-leaf
continuum
must
be
characterized
as
a
function
of
Win
the
continuum.
This
requires
taking
the
continuum
apart
to
characterize
the
P
responses
of
each
important
component,
and
then
putting
it
back
together
again
to
estimate
the
response
of
the
entire
continuum.
Yi-DEPENDENT
HYDRAULIC
CONDUCTIVITIES
IN
THE
CONTINUUM
In
analysing
the
components
of
the
soil-leaf
continuum,
it
is
useful
to
distinguish
conductance
(k)
from
conductivity
(K):
k
=WAY'
(
1
)
K
=
-QAdY-
dx)
(2)
The
Q
is
the
volume
flow
rate,
Pis
the
component
of
water
potential
driving
the
flow
(pressure
in
soil
and
xylem),
and
x
is
distance
along
the
flow
path.
In
tissues
where
more
than
one
P
component
participates
in
driving
Q
there
will
be
additional
terms
(e.g.
pressure
and
osmotic
components
in
extra-xylary
root
tissue;
Steudle
1994).
The
k
can
be
mea-
sured
directly,
or
derived
from
the
integration
of
K
with
respect
to
x
along
the
flow
path.
The
k
is
thus
a
function
of
flow
path
length,
whereas
K
is
independent
of
length.
In
addition,
k
and
K
are
usually
expressed
relative
to
an
area
transverse
to
the
flow
path,
which
can
be
designated
by
sub-
script.
Here,
we
use
a
subscript
s
for
soil
area
(e.g.
K
s
),
r
for
surface
area
of
absorbing
roots
(e.g.
K
r
),
and
x
for
xylem
cross-sectional
area
(e.g.
K,).
Plant
and
soil
K-values
are
not
constants,
but
depend
on
a
number
of
factors
ranging
from
temperature,
ionic
strength
of
the
transpiration
stream,
cell
membrane
com-
position,
and
the
driving
force
itself.
The
curves
of
Fig.
1
are
the
result
of
interactions
between
K
and
W,
and
we
confine
ourselves
to
this
source
of
variation
in
K
in
the
next
two
sections.
Soil
and
xylem
Together,
the
soil
and
xylem
account
for
probably
over
99%
of
the
total
length
of
the
flow
path
from
soil
water
source
to
evaporating
surface
in
the
leaf
even
in
the
small-
est
vascular
plants.
The
K(
V-
1
)
functions
of
soil
and
xylem
are
the
most
unambiguous
cause
of
the
hydraulic
limit
to
plant
water
use
as
defined
in
Fig.
1,
and
they
have
the
same
physical
basis
(Fig.
2).
Bulk
flow
in
both
media
occurs
through
pores
and
is
driven
by
a
gradient
in
pressure,
usu-
ally
a
negative
pressure
(included
in
the
`matric
potential'
for
soil).
The
pores
in
soil
are
the
highly
irregular
spaces
between
the
individual
soil
particles
(Fig.
2a)
whereas
pores
in
xylem
are
organized
into
the
relatively
wide
lumina
of
the
xylem
conduits
alternating
with
the
narrower
channels
of
the
connecting
pits
(Fig.
2b).
The
saturated
K
of
both
media
(K
at
P
near
0
with
all
pores
filled
with
water)
is
a
function
of
the
pore
dimensions.
Coarser
textured
soils
with
larger
particle
sizes
have
larger
pores
and
higher
saturated
K
s
than
finer
soils
(Jury,
Gardner
&
Gardner
1991).
Simi-
larly,
xylem
with
larger
diameter
and
longer
conduits
has
greater
K
x
than
xylem
with
narrower
and
shorter
conduits
(Zimmermann
1983).
The
permeability
of
the
pits
also
influences
the
saturated
K
x
(Petty
&
Puritch
1970;
Calkin,
Gibson
&
Nobel
1986).
As
might
be
expected
based
on
the
differences
in
pore
structure,
saturated
xylem
K
x
tends
to
be
greater
(e.g.
500
mol
s
4
m
-1
MPa
-1
for
diffuse-porous
Betula
occidentalis
Sperry
&
Saliendra
1994)
than
satu-
rated
soil
K
s
(e.g.
22
mol
s'
mp
-
a
1
for
a
loam;
Campbell
1985).
As
the
pore
water
pressure
becomes
more
negative
in
soil
and
xylem,
air
is
sucked
into
the
pore
space,
displacing
the
water,
ultimately
reducing
the
K
from
relatively
large
values
at
saturation
to
near
zero.
In
soil,
the
air
spreads
through
the
continuum
of
irregular
pore
space
(Fig.
2a),
and
the
nature
of
the
K(
V-
1
)
function
depends
on
soil
tex-
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
(c)
Porous
Fine
(Negative)
-
7
Soil
W(matric
potential)
(d)
Resistant
Vulnerable
0
0
(Negative)
Xylem
(pressure)
254
J.
S.
Spenyet
al.
(a)
Soil
article
Air
Water
‘).
Air,P=O
-
Water,
P
«0
Interconduit
pit
0
Figure
2.
Basis
for
variable
hydraulic
conductivity
(K)
in
soil
and
xylem.
(a)
Water
(shaded)
held
in
soil
pore
space
under
negative
pressure
(Y;
ignoring
osmotic
potential)
by
capillary
forces.
As
the
W
becomes
more
negative,
air
displaces
the
water-filled
pore
space
as
capillary
forces
yield
(from
Nobel
1991).
(b)
Water
(shaded)
is
held
in
xylem
conduits
under
negative
pressure
(P)
by
capillary
forces
in
pores
of
the
conduit
walls.
Some
conduits
are
inevitably
air
filled
owing
to
ageing,
abscission
of
parts,
and
damage.
As
P
becomes
more
negative,
air
spreads
to
adjacent
conduits
as
capillary
forces
yield
in
the
interconduit
pits
(inset).
Air
entry
nucleates
cavitation
and
reduces
xylem
conductivity
(modified
from
Cruiziat
&
Tyree
1990).
(c)
Declining
soil
conductivity
(K
s
,
per
soil
area)
as
a
function
of
increasingly
negative
soil
W.
Porous
soils
have
greater
saturated
K
s
,
but
more
precipitous
K(7
1
)
functions
than
finer
soils
because
their
larger
pore
spaces
empty
abruptly
at
less
negative
W.
(d)
Declining
xylem
conductivity
(K,
per
xylem
area)
as
a
function
of
increasingly
negative
W
(pressure)
of
xylem
water.
Vulnerable
xylem
loses
K„
at
less
negative
W
than
resistant
xylem
because
of
leakier
interconduit
pits.
Any
trade-off
between
cavitation
resistance
and
saturated
K„
is
minimized
by
the
potential
uncoupling
of
conduit
lumen
size
from
pit
structure.
ture.
Coarse
soils
with
large
pore
spaces
and
high
saturated
K
s
tend
to
show
a
much
more
abrupt
decline
in
K
s
with
P
than
finer-textured
soils
with
lower
saturated
K
s
(Fig.
2c;
Jury
et
al.
1991).
In
the
xylem,
the
air
spreads
conduit-by-
conduit
through
the
limiting
membranes
of
the
interconduit
pits
(Fig.
2).
The
air
'seeds'
cavitation
in
a
conduit
as
it
is
sucked
across
the
pit
membrane
the
details
of
the
seeding
process
depending
on
variations
in
pit
structure
between
angiosperms
and
conifers
(Crombie,
Hipkins
&
Milburn
1985;
Sperry
&
Tyree
1988;
Sperry
&
Tyree
1990;
Jarbeau,
Ewers
&
Davis
1995;
Sperry
et
al.
1996).
The
pressure
at
which
the
K
x
declines
in
xylem
depends
on
the
permeability
of
the
pits
rather
than
on
the
dimensions
of
the
conduit
lumina:
cavitation-resistant
xylem
has
less
permeable
pits
than
cavitation-susceptible
xylem
(Figs
2b
&
d).
Because
the
size
of
the
conduit
lumina
can
be
uncoupled
from
pit
structure,
there
is
no
necessary
relationship
between
satu-
rated
K
x
and
the
cavitation
resistance
(Fig.
2d),
although
this
can
occur
in
some
cases
(Tyree,
Davis
&
Cochard
1994a).
The
K(V-I)
function
of
xylem
is
often
referred
to
as
a
`vulnerability
curve'.
Living
tissues
of
root
and
leaf
In
terms
of
distances
involved,
the
living
tissues
of
root
and
leaf
are
trivial
components
of
the
soil—leaf
pathway.
These
short
distances
are
a
good
thing
for
the
plant
because
the
K
r
for
the
radial
flow
path
from
soil
to
xylem
of
absorbing
root
tissue
(approximately
0.0025
mmol
s-1
m-1
m—
ra
-
1
,
estimated
from
Steudle
&
Heydt
1997)
is
seven
to
eight
orders
of
magnitude
less
than
the
saturated
K
x
of
xylem
or
K
s
of
soil.
Do
Vtinduced
declines
in
tissue
K
contribute
to
a
poten-
tial
hydraulic
limitation
as
for
soil
and
xylem?
The
short
answer
is
probably
not,
because
there
is
no
evidence
for
the
direct,
instantaneous,
and
inevitable
coupling
between
tis-
sue
K
and
Pas
seen
for
K
and
Win
soil
and
xylem
(Fig.
2).
There
are
many
reasons
why
root
tissue
K
will
change
with
transpiration
and
W,
including
changes
in
membrane
con-
ductivity,
exo-
and
endo-dermal
permeability,
cell
and
root
shrinkage
(Nobel
1994;
Steudle
&
Peterson
1998).
How-
ever,
these
factors
are
potentially
controlled
by
metabolism,
and
their
linkage
to
Pis
poorly
characterized
and
likely
to
be
highly
variable
with
an
unpredictable
response
time.
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
Water
deficits
and
hydraulic
limits
to
leaf
water
supply
255
EVALUATING
HYDRAULIC
LIMITS
IN
THE
SOIL-LEAF
CONTINUUM
To
evaluate
the
'P-induced
changes
in
the
soil-leaf
contin-
uum,
the
various
K(P)
functions
need
to
be
integrated
over
the
entire
flow
path.
This
is
where
the
branching
structure,
root
depth
distribution,
root
:
shoot
ratio,
and
overall
size
of
the
continuum
becomes
important.
For
example,
the
fact
that
root
tissue
K
r
is
eight
orders
of
magnitude
less
than
xylem
lc
and
seven
orders
of
magnitude
less
than
saturated
soil
K
s
may
suggest
that
leaf
water
supply
is
predominately
controlled
by
root
tissue
hydraulics.
However,
in
a
medium-
sized
tree
the
distance
that
water
must
travel
through
xylem
and
soil
is
about
five
orders
of
magnitude
greater
than
in
crossing
the
root
tissue,
and
owing
to
the
branched
struc-
ture
of
the
root
system,
the
absorbing
root
surface
area
is
another
several
orders
of
magnitude
greater
than
the
trans-
verse
sectional
area
of
the
xylem
draining
these
roots.
Cou-
pled
with
the
substantial
decline
in
xylem
and
soil
K
with
V-
1
,
soil
and
xylem
components
can
exert
a
major
influence
on
leaf
water
supply,
particularly
under
drought
conditions.
The
importance
of
plant
size
is
evident
from
the
observed
decline
in
soil-leaf
hydraulic
conductance
with
tree
height
(Saliendra
et
al.
1995;
Mencuccini
&
Grace
1996);
this
decline
is
attributable
to
increasing
xylem
flow
distances,
since
the
distance
across
the
root
cortex
or
leaf
mesophyll
is
relatively
constant
for
all
plants.
Of
particular
importance
in
scaling
from
K
values
to
k
values
is
the
root
:
leaf
area
ratio
(A
R
:
A
L
).
This
influences
the
relative
importance
of
soil
versus
plant
limitations
on
water
uptake.
If
one
root
is
supplying
the
transpiration
stream
to
1000
leaves,
there
will
be
very
steep
V'
gradients
as
soil
water
funnels
down
to
the
limited
root
surface
area,
resulting
in
'dry
zones'
and
very
low
soil
K
in
the
rhizo-
sphere
that
can
limit
water
uptake
(Cowan
1965;
Newman
1969;
Williams
1974;
Caldwell
&
Richards
1986;
Passioura
1988).
Rhizosphere
dry
zones
will
also
be
favoured
in
porous
soils
with
more
sensitive
K(V-
1
)
functions
(Newman
1969).
Water
depletion
zones
around
roots
have
been
observed
using
magnetic
resonance
imaging
methods
and
computer-assisted
tomography
(Hainsworth
&
Aylmore
1989;
Macfall,
Johnson
&
Kramer
1990).
Both
modelling
and
empirical
approaches
have
been
used
to
assess
changes
in
continuum
k
with
V!
Empirical
methods
are
plagued
by
the
difficulties
of
measuring
con-
ductances
in
different
continuum
components
without
altering
them
in
the
process.
Two
common
methods
for
measuring
whole
shoot
or
root
system
k,
the
root
pressure
chamber
(Markhart
&
Smit
1990)
and
the
high
pressure
flow
meter
(Tyree
et
al.
1993b),
use
significant
positive
pres-
sures
over
extended
time
periods.
These
pressures
refill
any
embolized
xylem
in
the
system,
and
cannot
be
used
to
assess
'P-induced
changes
in
k.
An
alternative
is
to
estimate
conductance
components
in
droughted
plants
from
mea-
surements
of
V'
and
E
at
steady
state.
Using
this
method,
Blizzard
and
Boyer
(Blizzard
&
Boyer
1980)
found
that
whereas
soil
and
plant
hydraulic
conductances
declined
in
concert
during
drought
in
soybean,
most
of
the
decline
in
plant
conductance
was
not
in
the
root
cortex
component,
but
in
the
xylem.
Independent
measurements
of
the
cavita-
tion
resistance
in
soybean
are
consistent
with
their
data
(Sperry
2000).
Modelling
approaches
can
increase
the
utility
of
limited
empirical
data
through
the
generation
of
well-defined
and
testable
hypotheses.
Although
there
are
a
vast
number
of
soil-plant-atmosphere
models,
relatively
few
incorporate
K(V-
1
)
behaviour
throughout
the
continuum.
Earlier
models
incorporated
these
functions
for
the
soil,
but
did
not
incor-
porate
K(P)
functions
for
plant
xylem
(Cowan
1965;
New-
man
1969;
Bristow,
Campbell
&
Calissendorff
1984).
Milburn
was
the
first
to
realize
that
cavitation
in
xylem
could
also
limit
plant
water
uptake
in
a
fashion
analogous
to
dry
zone
formation
in
the
rhizosphere
(Milburn
1979).
The
xylem
limitation
was
analysed
quantitatively
in
1988
(Tyree
&
Sperry
1988)
after
methods
had
been
developed
to
measure
vulnerability
curves
(Sperry
1986).
In
the
1988
paper
it
was
shown
for
the
first
time
that
xylem
cavitation
could
underlie
stomatal
regulation
of
gas
exchange
in
response
to
transpiration-induced
water
stress.
A
model
was
presented
predicting
E
crit
on
the
basis
of
vulnerability
curves.
The
maximum
E
of
four
tree
species
closely
approached
suggesting
hydraulic
limits
on
stomatal
regulation.
A
large
number
of
less
quantitatively
developed
studies
have
since
supported
this
conclusion
by
showing
that
excessive
cavitation
would
occur
in
the
absence
of
sto-
matal
regulation
of
V'
(Tyree
&
Sperry
1988;
Meinzer
&
Grantz
1990;
Lu
et
al.
1995;
Saliendra
et
al.
1995;
Cochard,
Breda
&
Granier
1996;
Mencuccini
&
Comstock
1997;
Lin-
ton,
Sperry
&
Williams
1998;
Sparks
&
Black
1999;
Bond
&
Kavanagh
1999;
Nardini
&
Salleo
2000;
Vogt
2001).
The
shortcoming
of
the
Tyree
and
Sperry
model
(Tyree
&
Sperry
1988)
was
that
it
did
not
incorporate
below-ground
constraints
which
makes
it
less
useful
for
understanding
responses
to
soil
drought.
Recently
the
above-
and
below-ground
constraints
on
leaf
water
supply
have
been
combined
in
a
model
that
pre-
dicts
the
E
versus
V'
trajectory
for
the
entire
soil-leaf
con-
tinuum
(Sperry
et
al.
1998;
see
also
Williams,
Bond
&
Ryan
2001).
This
model
incorporates
KM
functions
of
soil,
root
xylem,
and
shoot
xylem,
and
it
can
account
for
branched
root
systems
penetrating
to
different
depths,
and
a
branched
canopy.
For
lack
of
well-defined
K(I')
behaviour
of
the
living
tissues
of
roots
and
leaves,
these
conductances
were
assumed
to
vary
to
the
same
extent
with
V'
as
xylem
and
thus
to
be
neither
more
nor
less
limiting.
Results
obtained
from
this
approach
are
synthesized
from
recent
publications
(Kolb
&
Sperry
1999;
Ewers,
Oren
&
Sperry
2000;
Hacke
et
al.
2000a;
Jackson,
Sperry
&
Dawson
2000)
in
the
following
sections
and
discussed
in
relation
to
empir-
ical
investigations.
The
water
use
envelope
and
plant
transpiration
Plotting
actual
water
use
envelopes
is
complicated
by
the
fact
that
bulk
soil
V'
varies
within
the
rooting
zone,
so
there
is
no
single
value
for
the
x-axis.
For
relatively
shallow-
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
256
J.
S.
Spenyet
al.
rooted
plants,
the
root
system
can
be
treated
as
a
single
layer,
with
pre-dawn
plant
Pused
as
an
average
bulk
soil
P
for
the
rooting
zone
(Sperry
et
al.
1998;
Kolb
&
Sperry
1999).
In
systems
where
soil
P
and
root
distribution
with
depth
is
important
and
known,
E
and
E
crit
can
be
estimated
for
any
soil
W
depth
distribution.
However,
the
results
can-
not
be
conveniently
plotted
as
a
single
water
use
envelope.
In
these
situations,
a
reference
envelope
can
be
derived
for
a
constant
bulk
soil
W
with
depth
(Ewers
et
al.
2000;
Hacke
et
al.
2000a),
or
the
soil
P
at
a
particular
depth
can
be
used
if
this
is
correlated
with
Pat
all
depths
(Jackson
et
al.
2000).
Another
complication
is
that
if
E
is
expressed
per
leaf
area,
variations
in
leaf
area
with
soil
moisture
will
change
the
envelope.
Depending
on
the
situation,
a
reference
leaf
area
can
be
used
(Sperry
et
al.
1998;
Kolb
&
Sperry
1999),
or
E
can
be
converted
to
ground
area
or
per
plant
basis
(Ewers
et
al.
2000;
Hacke
et
al.
2000a).
Model
predictions
of
the
envelope
show
considerable
variation
within
a
species
according
to
species'
cavitation
resistance
(Fig.
3a,
solid
Ecru
lines),
soil
type
(Fig.
3b),
root
:
shoot
ratio
(Ewers
et
al.
2000),
and
root
depth
distribution
(Jackson
et
al.
2000).
In
general,
vulnerable
xylem,
porous
soils,
low
root
:
shoot
ratio
and
shallow
root
systems
result
in
a
much
narrower
water
use
envelope
(less
negative
extraction
limit)
than
the
converse
properties.
The
variation
in
the
envelope
corresponds
with
habitat
and
with
mode
of
stomatal
regulation.
Importantly,
actual
plant
water
use
does
appear
to
'push
the
envelope',
partic-
ularly
under
drought
conditions
where
E
cfit
approaches
zero
(Fig.
3,
compare
Ecru
to
E).
Betula
occidentalis
(Fig.
3a,
water
birch)
is
a
small
tree
of
perennially
wet
riparian
hab-
itats
where
W
soil
is
constant
and
high.
It
has
a
very
narrow
envelope
on
account
of
its
vulnerable
xylem.
It
also
shows
isohydric
P
regulation,
keeping
midday
P
constant
and
above
a
W
ent
of
—1.7
MPa
despite
variations
in
soil
moisture,
humidity,
or
hydraulic
conductance
(Saliendra
et
al.
1995).
It
tends
to
maintain
relatively
small
margins
of
safety
from
E
ent
,
on
the
order
of
a
few
mmol
s
1
nr
2
,
even
under
well-
watered
conditions
(Fig.
3a).
This
plant
simply
does
not
have
'room'
for
anisohydric
W
regulation,
because
it
is
so
limited
by
its
high
W
ent
that
is
set
by
the
point
of
complete
cavitation
in
the
shoot
xylem.
Artemisia
tridentata
(Fig.
3a,
sagebrush)
is
a
shrub
of
desert
regions
where
soil
P
can
drop
below
—6
MPa.
It
has
a
much
broader
envelope
than
B.
occidentalis
owing
to
much
more
cavitation-resistant
xylem.
It
also
shows
aniso-
hydric
stomatal
regulation:
midday
leaf
P
drops
as
soil
moisture
declines,
at
least
until
midday
P
approaches
W
ent
during
drought
(Kolb
&
Sperry
1999).
This
anisohydric
reg-
ulation
results
in
very
large
safety
margins
from
E
crit
when
soil
P
is
high.
Thus,
drought-adapted
plants
with
greater
cavitation
resistance
and
broad
envelopes
appear
to
be
over-built
under
well-watered
conditions.
This
suggests
there
may
be
relatively
little
stomatal
control
in
these
plants
when
soil
is
wet,
with
maximum
E
and
minimum
leaf
P
being
limited
only
by
maximum
stomatal
apertures
and
densities.
Interestingly,
A.
tridentata
changes
its
cavitation
resistance
seasonally,
being
more
vulnerable
during
the
wet
spring,
and
becoming
more
resistant
with
the
onset
of
sum-
mer
drought
(Kolb
&
Sperry
1999).
The
broadest
envelope
(based
on
maximum
cavitation
resistance)
is
shown
in
Fig.
3a,
which
exaggerates
safety
margins
under
wet
conditions.
At
first
glance,
Fig.
3a
seems
to
imply
that
sagebrush
can
potentially
use
water
at
a
greater
rate
than
water
birch
under
wet
soil
conditions.
Although
this
is
correct
at
the
leaf
level,
to
the
extent
that
sagebrush
has
a
lower
leaf
area
per
plant
than
birch,
the
difference
in
E
crit
on
a
per
plant
or
stand
basis
between
the
species
diminishes.
The
envelopes
in
Fig.
3b
are
for
half-sib-related
planta-
tions
of
Pinus
taeda
(loblolly
pine),
and
illustrate
the
impor-
Variation
in
water
use
envelopes
(a)
(b)
Loblolly
pine
6
Sagebrush
/
Eat
4
---
E
/
/
/
z
/
Water
birch
2
/
Sand
0
-3
-2
0
-3
-2
Bulk
Soil
'I'
(MPa)
Figure
3.
Variation in
water
use
envelopes
and
actual
plant
water
use.
(a)
The
effect
of
differences
in
cavitation
resistance
between
species.
Sagebrush
plants
(Artemisia
tridentata)
with
more
cavitation-resistant
xylem
have
a
much
broader
water
use
envelope
than
vulnerable
species
like
water
birch
(Betula
occidentalis).
Soil
type
was
similar
between
both
species.
Actual
water
use
(dashed
lines)
converges
on
hydraulic
limits
(solid
curves),
particularly
under
drought
(from
Sperry
et
a1.
1998;
Kolb
&
Sperry
1999).
(b)
The
effect
of
soil
porosity
on
envelopes
for
half-sib
loblolly
pine
(Pinus
taeda)
plantations
of
equal
ages
(Hacke
et
al.
2000a).
Trees
in
sand
have
much
narrower
envelopes
(solid
curves)
than
trees
in
loam
owing
to
the
more
precipitous
K(T)
function
for
sandy
soil.
In
both
soils,
actual
water
use
(dashed
curves)
converged
on
hydraulic
limits
during
drought.
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
15
E
l y
-,5
10
9
t
5
03
'
0
.
3
4
GL
E
9
O
FL
Water
deficits
and
hydraulic
limits
to
leaf
water
supply
257
tance
of
soil
type.
Trees
growing
in
sand
had
a
much
narrower
envelope
than
those
in
the
finer
loam
soil
because
of
the
more
sensitive
K(P)
function
of
sand
(e.g.
Fig.
2c).
The
actual
water
use
in
these
plantations
was
adjusted
to
stay
within
the
corresponding
envelopes,
converging
on
E
crit
under
drought
(Fig.
3b,
dashed
lines).
The
broader
enve-
lope
in
loam
was
associated
with
an
isohydric
regulation
of
midday
leaf
V'
at
approximately
—24
MPa;
the
narrower
envelope
in
sand
corresponded
with
a
less
negative
isohy-
dric
regulation
at
approximately
—F6
MPa
(Hacke
et
al.
2000a).
Importantly,
where
model
predictions
of
E
have
been
compared
with
actual
E
measurements,
the
agreement
is
very
good
whether
for
greenhouse
plants
subjected
to
short-term
rapid
drought
of
days
(Sperry
et
al.
1998),
sage-
brush
shrubs
subjected
to
a
prolonged
monotonic
summer
drought
(Kolb
&
Sperry
1999),
or
for
loblolly
pine
trees
experiencing
irregular
drought
cycles
spanning
two
grow-
ing
seasons
(Hacke
et
al.
2000a).
These
results
are
encour-
aging,
because
they
suggest
that
the
changes
in
soil
and
xylem
K
with
drying
are
important
causes
of
change
in
the
overall
soil—leaf
k.
If
the
model
can
successfully
predict
E,
it
also
gives
more
credence
to
its
predictions
of
E
crit
,
which
are
more
difficult
to
validate.
Do
plants
ever
exceed
E
ent
and
trigger
complete
loss
of
hydraulic
connection
to
all
or
part
of
the
canopy?
Fig.
3
sug-
gests
that
this
would
be
most
likely
to
occur
under
soil
drought
situations
where
E
converges
on
E
cru
.
Transport
failure
has
been
associated
with
foliar
desiccation
in
ripar-
ian
cottonwoods
subject
to
experimental
soil
drying
or
nat-
ural
drought
in
floodplains
subject
to
declining
water
tables
(Tyree
et
al.
1994b;
Sparks
&
Black
1999;
Rood
et
al.
2000).
Drought
deciduous
behaviour
in
walnut
(Juglans
regia)
has
also
been
attributed
to
excessive
cavitation
in
the
leaves
(Tyree
et
al.
1993a).
Desiccation
by
hydraulic
failure
has
also
been
postulated
for
chaparral
shrubs
(Ceanothus
cras-
sifolius)
exposed
to
more
than
6
months
of
drought
and
weeks
of
drying
winds
(Davis
et
al.
2002;
Davis,
Kolb
&
Barton
1998).
Seedling
mortality
in
the
chaparral
has
been
linked
to
excessive
cavitation
(Williams,
Davis
&
Portwood
1997).
Recent
dry
growing
seasons
in
the
Great
Basin
have
also
caused
complete
transport
failure
in
roots
and
foliage
loss
in
desert
shrubs
(Chrysothamnus
viscidiflorus,
Sperry
and
Hacke,
unpublished).
We
suspect
that
more
instances
of
dieback
by
hydraulic
failure
will
be
reported
as
investi-
gators
become
more
aware
of
the
phenomenon.
Causes
of
hydraulic
limitation
The
question
of
where
the
limiting
hydraulic
resistances
are
in
the
soil—leaf
continuum
has
long
been
a
matter
of
debate
(Gardner
1965;
Newman
1969;
Molz
1975;
Blizzard
&
Boyer
1980).
The
water
use
envelope
is
defined
by
a
limit-
ing
resistance
a
resistance
somewhere
in
the
continuum
that
goes
to
infinity.
Which
component
is
most
limiting
and
under
what
circumstances?
A
theoretical
answer
is
pro-
vided
by
Fig.
4,
and
it
suggests
that
the
limiting
component
can
be
a
number
of
places
depending
on
the
circumstances.
.---
Water
birch
-
2
---------
Sand
-
Boxelder
Lo
sand
I
1),
N
__
-6
\
°
N
Sagebrush
c
\
N.
-8
\
"---.
-10
\
\
V
r
,
vt
...
i
.
..
41'
N,
\
.
s
..
,
,
----.
\\
-
12
\TS'
\\
Ceanothus
---.
---,
----.
-14
\
----
---,
I
i
\
14
(a)"
-
--...
10
20
30
40
Root-to-leaf
area
ratio
(A
R
:A
L
)
Loam
100
o.
0
Sand
0
80
E
ri
E
60
/
4
4
9
40
o
1 1
10
Root-to-leaf
area
ratio
(A
R
:A
L
)
Figure
4.
Interactions
between
soil
type,
xylem
type,
and
root
:
leaf
ratio
on
predicted
hydraulic
limits
to
plant
water
use.
(a)
Extraction
limit
(bulk
soil
Pat
E
c
fit
•=--
0)
versus
root
:
leaf
area
ratio
(A
R
:
A
L
).The
dashed
curves
for
the
indicated
soils
assume
that
the
rhizosphere
alone
limits
water
extraction
(i.e.
no
xylem
cavitation).
Solid
horizontal
lines
represent
the
xylem
pressure
causing
100%
cavitation
in
the
indicated
species
(water
birch,
Betula
occidentalis;
box
elder,
Acer
negundo;
sagebrush,
Artemisia
tridentata;
ceanothus,
Ceanothus
crassifolius).
The
extraction
limit
for
a
soil
plus
xylem
combination
is
found
by
crossing
over
from
the
soil
curve
to
the
xylem
line
as
A
R
:
AL
increases
(e.g.
circles
for
sandy
loam
+
sagebrush).
From
Sperry
et
al.
(1998).
(b)
Extraction
potential
(=
area
under
the
water
use
envelope)
versus
root—leaf
area
ratio
(A
R
:
A
L
)
for
half-sib
related
loblolly
pines
(Pinus
taeda)
in
two
even-aged
plantations.
Symbols
are
measured
values
of
A
R
:
AL.
Extraction
limit
is
shown
relative
to
its value
at
A
R
:
AL
of
40,
a
liberal
maximum
for
woody
plants.
Low
A
R
:
AL
limits
extraction
because
of
hydraulic
failure
initiated
in
the
rhizosphere.
Extraction
at
high
A
R
:
AL
is
limited
by
xylem
cavitation.
Trees
in
sandy
soil
maintained
a
similar
relative
extraction
potential
as
in
loam
by
increasing
their
A
R
:
AL
to
minimize
the
rhizosphere
limitation
(Hacke
et
al.
2000a).
Figure
4a
shows
the
interaction
between
the
extraction
limit
'width'
of
the
water
use
envelope,
or
the
permanent
wilting
point)
and
the
A
R
:
A
L
ratio
for
different
soil
types
(curved
dashed
lines)
and
cavitation
resistances
(solid
hor-
izontal
lines).
The
extraction
limit
for
any
soil
plus
xylem
combination
is
found
by
crossing
from
the
soil
curve
to
the
xylem
line
as
A
R
:
A
L
increases
(e.g.
circles
for
sandy
loam
(b)
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251
-
263
258
J.
S.
Spenyet
al.
+
sagebrush
xylem).
As
A
R
:
A
L
increases
from
zero,
the
extraction
limit
decreases
because
the
greater
root
area
for
water
uptake
relieves
a
hydraulic
limitation
at
the
rhizo-
sphere.
Above
a
threshold
A
R
:
A
L
,
there
is
no
further
decrease
in
the
extraction
limit
because
at
this
point
the
limiting
resistance
has
shifted
from
the
rhizosphere
to
the
xylem
as
a
result
of
cavitation
(Sperry
et
al.
1998).
The
shift
from
rhizosphere
to
xylem
limitation
is
gradual,
with
an
intermediate
A
R
:
A
L
range
where
both
are
colimiting.
As
expected
from
previous
analyses
(Newman
1969;
Bristow
et
al.
1984;
Passioura
1988),
Fig.
4a
confirms
that
a
rhizo-
sphere
limitation
is
probably
only
a
serious
factor
in
soils
coarser
than
a
loam.
In
loam
or
finer
soils,
hydraulic
limits
will
be
set
by
cavitation
resistance
of
the
xylem
for
even
very
low
A
R
:
A
L
.
In
these
cases,
a
more
negative
extraction
limit
results
from
a
greater
cavitation
resistance.
The
interaction
between
A
R
:
A
L
and
the
water
use
enve-
lope
is
also
shown
in
Fig.
4b
for
the
loblolly
pine
(P.
taeda)
stands
of
different
soils
shown
in
Fig.
3b.
In
this
figure,
the
envelope
is
represented
by
the
area
under
the
E'
en
,
curve
(`extraction
potential').
The
extraction
potential
is
a
more
sensitive
measure
of
hydraulic
limits
than
just
the
extrac-
tion
limit,
because
it
reflects
changes
in
the
latter
as
well
as
the
restriction
of
E'
en
,
within
the
water
use
range.
This
term
should
not
be
misconstrued
as
predicting
the
potential
amount
of
water
extracted.
The
envelope
by
itself
only
pre-
dicts
the
maximum
steady-state
rate
of
extraction
as
a
func-
tion
of
bulk
soil
P.
Once
again,
a
threshold
A
R
:
A
L
is
evident
above
which
further
increases
do
not
increase
the
size
of
the
envelope
because
once
the
rhizosphere
limita-
tion
is
relieved,
the
xylem
limitation
is
not
influenced
by
adding
more
roots.
The
A
R
:
A
L
threshold
is
shifted
much
higher
in
sand
versus
loam
soil
because
the
much
more
sen-
sitive
K(P)
function
in
the
coarser
soil
exacerbates
the
rhizosphere
limitation
problem.
Interestingly,
the
actual
A
R
:
A
L
of
these
plants
was
close
to
the
optimal
threshold
value
in
both
stands
(Fig.
4b,
symbols
on
curves),
which
required
a
much
greater
root
investment
in
the
sandy
soil.
Fertilizing
plants
often
results
in
a
reduction
in
the
root
:
shoot
ratio
(Linder
et
al.
1987;
Haynes
&
Gower
1995;
Albaugh
et
al.
1998),
which
according
to
Fig.
4b
could
restrict
the
water
use
envelope
and
render
fertilized
plants
more
vulnerable
to
drought.
A
fertilizing
treatment
of
the
sand-grown
loblolly
pines
shown
in
Fig.
4b
did
in
fact
result
in
a
significant
reduction
in
A
R
:
A
L
whether
or
not
the
fer-
tilized
stands
were
also
irrigated
(Ewers
et
al.
2000).
When
irrigation
was
applied
in
addition
to
fertilization,
there
was
a
substantial
narrowing
of
the
water
use
envelope,
predict-
ing
that
these
trees
would
be
relatively
sensitive
to
drought
in
the
event
that
irrigation
was
withdrawn.
This
kind
of
response
may
explain
greater
drought-sensitivity
of
fertil-
ized
stands
seen
in
other
studies
(Linder
et
al.
1987).
Inter-
estingly,
the
non-irrigated
but
fertilized
trees
showed
much
less
of
a
narrowing
of
the
envelope
because
the
root
xylem
showed
an
increase
in
cavitation
resistance
that
tended
to
counter
the
loss
or
A
R
:
A
L
(Ewers
et
al.
2000).
When
the
root
:
shoot
ratio
is
sufficiently
high
to
cause
hydraulic
failure
in
the
xylem,
where
in
the
xylem
does
it
occur?
In
the
simple,
but
less
realistic,
situation
where
there
is
one
K(V-
1
)
function
for
all
the
xylem
from
root
to
leaf,
fail-
ure
will
occur
only
at
the
distal
end
of
the
flow
path
where
Pis
most
negative.
Under
these
conditions,
the
Vi
crit
and
the
extraction
limit
are
both
equal
to
the
V'
causing
complete
cavitation
in
the
xylem.
However,
in
many
woody
plants,
the
root
xylem
is
substantially
more
vulnerable
to
cavita-
tion
than
shoot
xylem
(Alder,
Sperry
&
Pockman
1996;
Sperry
et
al.
1998;
Kolb
&
Sperry
1999;
Ewers
et
al.
2000;
Hacke
et
al.
2000a;
Hacke,
Sperry
&
Pittermann
2000b).
The
model
predicts
that
hydraulic
failure
in
this
case
can
occur
in
the
root
system
(Kolb
&
Sperry
1999;
Ewers
et
al.
2000;
Hacke
et
al.
2000a).
Roots
in
the
shallowest
soil
layers
will
lose
transport
capacity
earliest
in
a
drought,
and
if
these
are
the
only
roots
supplying
the
canopy,
their
failure
will
trigger
failure
in
the
distal
shoot
xylem
as
well.
In
this
case,
the
Vi
crit
and
extraction
limit
is
the
V'
causing
complete
cavitation
in
the
more
vulnerable
root
xylem
(Kolb
&
Sperry
1999).
If
deeper
roots
are
present,
failure
in
shallow
roots
will
simply
shift
water
uptake
down
to
wetter
soil
layers
without
necessarily
triggering
shoot
damage.
To
some
degree,
the
architecture
of
the
plant
may
be
localizing
the
point
of
hydraulic
failure
to
redundant
and
replaceable
points
in
the
continuum,
thereby
increasing
its
ability
to
cope
during
progressive
soil
drought
and
to
recover
once
it
is
relieved.
This
was
the
essence
of
M.H.
Zimmermann's
'segmentation
hypothesis'
proposed
many
years
ago
(Zimmermann
1983).
By
analogy
with
an
electric
circuit,
it
makes
sense
for
the
plant
to
limit
failure
to
redun-
dant
components
that
are
readily
replaceable
(`hydraulic
fuses')
rather
than
to
have
it
disrupt
the
major
transport
arteries.
Hydraulic
limits
and
optimal
plant
water
use:
testable
hypotheses
The
above
sections
suggest
that
plants
have
co-ordinated
their
hydraulic
capacity,
as
quantified
in
the
water
use
enve-
lope,
to
match
their
mode
of
V'
regulation.
They
invest
as
much
in
roots
and
cavitation
resistance
as
is
necessary
for
their
particular
water
use
niche,
presumably
because
to
invest
more
would
be
a
waste
of
carbon.
The
cost
of
excess
roots
is
obvious,
but
what
is
the
cost
of
excess
cavitation
resistance?
Recently,
the
cost
of
cavitation
resistance
has
been
mechanistically
linked
to
wood
density:
denser
and
stronger
wood
is
necessary
to
balance
the
greater
negative
pressure
within
the
xylem
conduits
(Hacke
et
al.
2001a).
Thus,
even
if
cavitation
resistance
was
not
always
associ-
ated
with
a
reduced
saturated
xylem
conductivity
(Tyree
et
al.
1994a),
it
would
exact
a
price
by
reducing
growth
rate
through
greater
xylem
density
(Enquist
et
al.
1999).
Figure
4,
although
not
cast
in
units
of
carbon
cost,
rep-
resents
a
beginning
for
quantifying
the
trade-offs
between
water
extraction
capability
versus
the
required
plant
invest-
ment.
It
allows
us
to
formulate
several
testable
hypotheses
for
how
plants
should
alter
their
morphology
and
physiol-
ogy
to
optimize
water
use
under
different
soil
and
climatic
conditions.
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
Water
deficits
and
hydraulic
limits
to
leaf
water
supply
259
1
To
the
extent
that
water
uptake
is
the
sole
driver
of
A
R
:
A
L
,
plants
should
adjust
their
A
R
:
A
L
to
the
threshold
value
where
the
rhizosphere
and
xylem
are
more
or
less
colimiting
(Fig.
4b).
An
A
R
:
A
L
below
this
threshold
would
compromise
extraction
capability,
and
an
A
R
:
A
L
above
this
threshold
would
be
ineffectual
for
increased
water
uptake.
2
To
the
extent
that
fertilizing
reduces
A
R
:
A
L
,
it
can
reduce
water
uptake
from
drying
soils
and
increase
drought
sensitivity
(Ewers
et
al.
2000).
3
Across
soil
types:
the
more
porous
the
soil,
the
higher
the
A
R
:
A
L
will
have
to
be
to
saturate
the
extraction
limit.
In
the
most
porous
soils
(e.g.
Fig.
4a,
sand,
loamy
sand),
cavitation
resistance
should
be
diminished
because
the
soil
dries
out
at
relatively
high
Wregardless
of
the
A
R
:
A
L
.
4
Within
a
given
soil
type:
the
drier
the
soil
of
the
rooting
zone,
the
more
cavitation-resistant
the
xylem
and
the
higher
the
A
R
:
A
L
for
saturating
the
extraction
limit.
5
For
a
seasonally
dry
soil
moisture
regime:
more
porous
soils
will
favour
greater
rooting
depth
than
finer
soils
because
less
water
will
be
available
for
extraction
at
low
Win
the
shallow
layers
of
a
porous
versus
fine
soil
(Jack-
son
et
al.
2000).
Most
of
these
hypotheses
have
received
some
support.
Figure
4b
is
evidence
for
1
and
3
wherein
the
A
R
:
A
L
of
half-sib
loblolly
pine
plantations
(symbols
on
loam
and
sand
curves)
increased
by
nearly
six-fold
to
stay
near
the
value
required
to
saturate
the
extraction
potential
in
response
to
growth
in
soils
of
very
different
porosity.
This
was
also
accompanied
by
a
reduction
in
cavitation
resis-
tance
of
sand-grown
versus loam-grown
trees
(Hacke
et
al.
2000).A
follow-up
study
on
fertilizing
treatments
suggested
hypothesis
2,
which
has
not
been
directly
tested
(Ewers
et
al.
2000a).
Hypothesis
4
has
been
supported
by
a
number
of
studies
showing
a
correlation
between
cavitation
resistance
and
the
minimum
xylem
P
experienced
by
plants
in
their
natural
habitats
(Tyree
&
Cochard
1996;
Davis
et
al.
1998,
1999;
Hacke
et
al.
2000b;
Pockman
&
Sperry
2000),
but
see
(Pinol
&
Sala
2000).
The
fifth
hypothesis
for
rooting
depth
was
recently
supported
in
comparisons
of
rooting
depths
across
soil
types
in
global
root
databases
(Jackson
et
al.
2000).
DISCUSSION
Implementing
the
theory
of
hydraulic
limitation
has
been
successful
in
predicting
the
regulation
of
transpiration
in
response
to
soil
moisture
and
soil
type
within
a
plant
type,
and
also
the
huge
differences
in
water
use
between
species.
The
W
regulation
of
stomata
does
appear
to
be
necessary
for
avoiding
hydraulic
failure,
and
thereby
maximizing
the
extraction
of
soil
water.
The
pattern
of
P
regulation
-
whether
it
is
isohydric
or
anisohydric,
and
the
particular
thresholds
of
Pthat
are
controlled
-
have
to
be
tuned
to
the
soil
moisture
regime
and
the
hydraulic
capability
of
the
plant's
root
system
and
xylem.
The
extensive
variation
in
water
use
between
plants
can
be
attributed
in
part
to
dif-
ferences
in
their
'hydraulic
equipment'
that
is
presumably
optimized
for
drawing
water
from
a
particular
temporal
and
spatial
niche
in
the
soil
environment.
Explicit
hypoth-
eses
for
this
optimization
can
be
tested
in
the
further
eval-
uation
of
the
hydraulic
approach.
We
can
only
speculate
on
how
the
plant
achieves
a
co-
ordination
between
the
stomatal
regulation
of
P
and
the
hydraulic
capabilities
of
the
soil-canopy
supply
line.
In
an
evolutionary
sense,
it
would
be
achieved
by
natural
selec-
tion
for
the
midday
leaf
Pthat
maximizes
gas
exchange:
a
P
at
a
safe
distance
above
W
ent
.
But
in
a
physiological
sense,
how
does
B.
occidentalis
(Fig.
3a)
'know'
to
keep
midday
leaf
W
above
its
W
ent
of
-1.7
MPa
that
is
set
by
its
cavitation
resistance,
and
to
thereby
stay
within
its
water
use
envelope
(Saliendra
et
al.
1995;
Sperry
et
al.
1998)?
If
the
signalling
system
between
living
cells
and
stomata
is
independent
of
cavitation
there
is
no
physiological
reason
why
midday
leaf
P
in
this
species
could
not
be
regulated
near
-0.5
MPa
or
near
-2.5
MPa,
although
either
value
would
be
maladaptive
-
the
former
by
unnecessarily
limiting
gas
exchange,
and
the
latter
by
causing
hydraulic
failure.
In
this
case,
the
observed
co-ordination
would
be
through
independent
adjustments
(via
natural
selection)
in
stomatal
regulation
and
transport
capacity.
Alternatively,
the
co-ordination
may
be
achieved
more
directly
via
a
physiological
link
between
cavitation
and
the
stomatal
signalling
system
as
suggested
by
Nardini
&
Salleo
(2000).
The
accuracy
of
the
predictions
of
water
use
and
hydrau-
lic
limits
depends
on
the
accuracy
of
the
K(P)
functions
along
the
flow
path,
particularly
of
the
most
limiting com-
ponent
in
series.
For
example,
a
recent
study
concluded
that
cavitation
resistance
of
conifers
in
the
north-western
United
States
did
not
correlate
with
water
availability
in
the
habitat
(Pinol
&
Sala
2000).
However,
only
stem
xylem
was
considered,
which
in
many
conifers
and
other
woody
plants
is
substantially
more
resistant
(and
not
limiting
to
water
uptake)
as
compared
to
root
xylem
(Sperry
&
Ikeda
1997;
Linton
et
al.
1998.;
Hacke
et
al.
2000a,b).
The
accuracy
of
soil
K(P)
functions
is
critical
in
more
porous
soils
where
a
rhizosphere
limitation
is
important.
These
soil
functions
are
nearly
impossible
to
measure
over
much
of
the
range
of
interest
for
plants
in
natural
communities
and
must
be
esti-
mated
from
other
soil
properties
(Campbell
1985).
It
has
recently
been
noted
that
hydraulic
limits
can
be
substan-
tially
influenced
by
the
length
of
the
xylem
conduits
as
well
as
their
K(V-
1
)
behaviour.
In
general,
the
longer
the
conduits
at
the
site
of
cavitation,
the
more
substantial
the
hydraulic
limitation
for
a
given
K(P)
relationship
(Comstock
&
Sperry
2000).
To
predict
the
response
of
plants
to
repeated
drying
and
wetting
cycles,
hysteresis
in
the
K(V-
1
)
functions
of
soil
and
xylem
must
be
known.
Although
there
is
significant
hyster-
esis
in
soil
K(P)
behaviour
(Philip
1966;
Campbell
1985),
this
is
probably
much
less
than
for
the
xylem
curves
depending
on
the
extent
and
mechanism
of
cavitation
reversal.
The
xylem
pressure
must
rise
to
near
atmospheric
or
above
before
gases
can
dissolve
(Yang
&
Tyree
1992),
©
2002
Blackwell
Science
Ltd,
Plant,
Cell
and
Environment,
25,
251-263
260
J.
S.
Spenyet
al.
meaning
there
should
be
a
substantial
hysteresis
in
theK(V)
behaviour
of
the
xylem.
Several
studies
have
demonstrated
this
refilling
when
xylem
pressure
is
within
30
kPa
of
atmo-
spheric
or
above
(Sperry
et
al.
1987;
Sperry,
Donnelly
&
Tyree
1988;
Borghetti
et
al.
1991;
Sperry
&
Sullivan
1992;
Cochard,
Ewers
&
Tyree
1994;
Sperry
et
al.
1994;
Hacke
&
Sauter
1996;
Zhu,
Cox
&
Arp
2000;
Cochard
et
al.
2001).
In
some
species,
the
K(V-
1
)
function
itself
can
be
altered
after
an
embolism
and
refilling
cycle
as
a
result
of
increased
per-
meability
of
the
vascular
system
to
air
entry
(Hacke
et
al.
2001b).
A
further
complication
is
the
possibility
that
xylem
conduits
may
refill
even
when
the
prevailing
pressure
in
the
transpiration
stream
is
substantially
negative
(Salleo
et
al.
1996;
Canny
1997;
McCully,
Huang
&
Ling
1998;
Zwien-
iecki
&
Holbrook
1998;
Holbrook
&
Zwieniecki
1999;
Tyree
et
al.
1999;
Zwieniecki
&
Holbrook
2000).
However,
these
results
are
equivocal
because
studies
using
cryo-SEM
techniques
to
assess
embolism
reversal
have
been
shown
to
be
subject
to
artifacts
(Cochard
et
al.
2000),
and
other
inves-
tigations
did
not
measure
xylem
pressure
during
the
refill-
ing
process
to
confirm
that
it
indeed
was
low
enough
to
require
a
novel
refilling
mechanism
(Salleo
et
al.
1996;
Zwieniecki
&
Holbrook
1998;
Tyree
et
al.
1999).
More
information
on
the
refilling
process
during
rewetting
cycles
is
required.
The
living
tissues
of
root
and
leaf
are
the
cause
of
vari-
able
conductances
which
could
have
a
significant
modulat-
ing
effect
on
the
physical
limitations
that
exist
in
the
soil
and
xylem
components.
Although
it
seems
unlikely
that
these
could
eliminate
hydraulic
limitations
set
by
soil
and
xylem,
these
plant-mediated
effects
could
significantly
alter
the
shape
of
the
E
versus
V'
trajectory
(Fig.
la)
over
the
short-term
(Tsuda
&
Tyree
2000),
and
cause
substantial
hysteresis
in
the
recovery
of
hydraulic
conductance
after
a
drought
(Nobel
1994).
An
additional
complication
are
reports
of
the
effects
of
ion
composition
of
the
xylem
sap
on
xylem
conductivity
(Zimmermann
1978;
Ieperen,
Meeteren
&
Gelder
2000;
Zwieniecki
et
al.
2001).
These
ion
effects
do
not
appear
to
influence
the
cavitation
resistance
of
the
xylem
(V.
Stiller,
J.S.
Sperry,
unpublished
data).
A
final
complication
linked
to
radial
water
movement
across
roots
is
the
build-up
of
solutes
external
to
the
endodermis
in
saline
and
heavily
fertilized
soils
which
can
reduce
water
uptake
in
a
manner
somewhat
similar
to
dry
zone
forma-
tion
at
the
rhizosphere
(Hamza
&
Aylmore
1992;
Stirzaker
&
Passioura
1996).
The
examples
we
have
discussed
have
been
limited
to
steady-state
conditions.
It
is
important
also
to
consider
non-
steady-state
conditions
in
a
spatially
explicit
soil—root
envi-
ronment
(e.g,
see
Doussan,
Vercambre
&
Pages
1998).
This
eliminates
the
somewhat
artificial
bulk
soil
versus
rhizo-
sphere
distinction
and
incorporates
the
pararhizal
resis-
tances
(Newman
1969)
that
govern
long-distance
water
flow
in
the
soil.
In
this
way,
the
'sphere
of
influence'
of
a
particular
plant
root
system
can
be
analysed,
along
with
competitive
interactions
between
plants.
Above
the
ground,
the
influence
of
stem
capacitance
on
hydraulic
lim-
itations
may
be
important
for
large
trees
where
the
decline
in
hydraulic
conductance
from
soil
to
leaf
may
be
limiting
carbon
gain
(Ryan
&
Yoder
1997).
The
overwhelming
limitation
on
plant
productivity
is
leaf
water
supply
(Kramer
&
Boyer
1995),
and
it
is
logical
that
factors
influencing
this
water
supply
play
a
central
role
in
the
adaptation
of
plants
to
their
terrestrial
environment.
Leaf
water
supply
is
much
more
complex
than
simply
the
water
availability
in
the
rooting
zone.
The
process
of
mov-
ing
water
to
the
site
of
evaporation
with
a
minimum
of
investment
is
a
major
factor
driving
the
architecture
and
physiology
of
land
plants,
including
the
function
of
stomatal
regulation.
In
this
context,
the
physiological
tolerance
of
cells
to
water
deficits
should
be
expected
to
match
the
sup-
ply
capacity
of
the
system
delivering
resources
to
these
cells.
Interestingly,
recent
work
does
show
that
the
sensitiv-
ity
of
leaf
cell
physiology
to
Wcorresponds
to
the
cavitation
resistance
of
the
xylem
(Brodribb
&
Hill
1999).
The
signif-
icance
of
vascular
supply
to
physiology
is
not
lost
on
the
armies
of
cardiovascular
physiologists
and
modellers.
Transport
issues
appear
to
be
similarly
important
in
the
evolution
and
functioning
of
plants.
ACKNOWLEDGMENTS
During
the
preparation
of
this
manuscript,
the
two
lead
authors
were
supported
in
part
by
NSF
grant
IBN-9723464.
J.C.
was
partially
supported
by
EPA
grant
no.
826531-01-0.
R.O.
was
supported
by
the
USDA
Forest
Service
through
the
Southern
Global
Change
Program,
and
the
US
Department
of
Energy
through
the
South-east
Regional
Center
at
the
University
of
Alabama
(Co-operative
Agreement
no.
DE-FC03-90ER61010).
We
thank
an
anonymous
reviewer
for
extensive
suggestions
that
we
feel
greatly
improved
the
final
manuscript.
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