Photosynthetic and Stomatal Responses of Two Mangrove Species, Aegiceras corniculatum and Avicennia marina, to Long Term Salinity and Humidity Conditions

Abstract

Gas exchange characteristics were studied in two mangrove species, Aegiceras corniculatum (L.) Blanco and Avicennia marina (Forstk.) Vierh. var australasica (Walp.) Moldenke, grown under a variety of salinity and humidity conditions. The assimilation rate was measured as a function of the intercellular CO(2) concentration [A(c(i)) curve]. The photosynthetic capacity decreased with increase in salinity from 50 to 500 millimolar NaCl, as shown by decline in both the initial linear slope and the upper plateau of the A(c(i)) curve, with A. corniculatum being the more sensitive species. The decline in photosynthetic capacity was enhanced by increase in the leaf to air vapor pressure difference from 6 to 24 millibars, but this treatment caused a decrease in only the upper plateau of the A(c(i)) curve. Stomatal conductance was such that the intercellular CO(2) concentration obtaining under normal atmospheric conditions occurred near the transition between the lower linear and upper plateau portions of the A(c(i)) curves. Thus, stomatal conductance and photosynthetic capacity together co-limited the assimilation rate, which declined with increasing salinity and decreasing humidity. The marginal water cost of carbon assimilation was similar in most treatments, despite variation in the water loss/carbon gain ratio.

Full text

Plant
Physiol.
(1
984)
74,
1-6
0032-0889/84/74/000
1/06/$0
1.00/0
Photosynthetic
and
Stomatal
Responses
of
Two
Mangrove
Species,
Aegiceras
corniculatum
and
Avicennia
marina,
to
Long
Term
Salinity
and
Humidity
Conditions'
Received
for
publication
April
13,
1983
and
in
revised
form
August
5,
1983
MARILYN
C.
BALL*
AND
GRAHAM
D.
FARQUHAR
P.O.
Box
475,
Department
of
Environmental
Biology,
Research
School
of
Biological
Sciences,
Australian
National
University,
Canberra,
ACT
2601
Australia
ABSTRACTI
MATERIALS
AND
METHODS
Gas
exchange
characteristics
were
studied
in
two
mangrove
species,
Aegiceras
cornicalatum
(L.)
Blanco
and
Avicennia
marina
(Forstk.)
Vierh.
var
australasica
(Walp.)
Moldenke,
grown
under
a
variety
of
salinity
and
humidity
conditions.
The
assimilation
rate
was
measured
as
a
function
of
the
intercellular
CO2
concentration
IA(c,)
curve].
The
photosynthetic
capacity
decreased
with
increase
in
salinity
from
50
to
500
millimolar
NaC1,
as
shown
by
decline
in
both
the
initial
linear
slope
and
the
upper
plateau
of
the
A(c;)
curve,
with
A.
corniculatum
being
the
more
sensitive
species.
The
decline
in
photosynthetic
capacity
was
en-
hanced
by
increase
in
the
leaf
to
air
vapor
pressure
difference
from
6
to
24
millibars,
but
this
treatment
caused
a
decrease
in
only
the
upper
plateau
of
the
A(cp)
curve.
Stomatal
conductance
was
such
that
the
intercellular
CO2
concentration
obtaining
under
normal
atmospheric
con-
ditions
occurred
near
the
transition
between
the
lower
linear
and
upper
plateau
portions
of
the
A(c;)
curves.
Thus,
stomatal
conductance
and
photosynthetic
capacity
together
co-limited
the
assimilation
rate,
which
declined
with
increasing
salinity
and
decreasing
humidity.
The
marginal
water
cost
of
carbon
assimilation
was
similar
in
most
treatments,
despite
variation
in
the
water
loss/carbon
gain
ratio.
Humidity
has
been
reported
to
modify
the
response
to
salinity
in
several
plant
species,
presumably
because
of
interactive
effects
of
these
factors
on
carbon
gain
in
relation
to
water
use
and
hence
also
ion
uptake.
With
increasing
salinity,
increasing
humidity
adversely
affected
the
growth
of
Atriplex
halimus,
a
halophyte
of
arid
regions
(
14),
but
ameliorated
the
reduction
in
growth
in
the
glycophyte,
Gossypium
hirsutum
(11),
and
in
the
mangroves,
Aegiceras
corniculatum
and
Avicennia
marina
(1).
The
decline
in
growth
rates
of
the
mangrove
species
with
increasing
salinity
and
decreasing
humidity
was
attributed
to
decrease
in
both
the
leaf
area/plant
mass
ratio
and
A2,
with
the
latter
being
the
major
factor
(1).
The
present
study
describes
the
influence
of
changes
in
stomatal
conductance
and
photosynthetic
metabolism
on
water
use
in
relation
to
carbon
gain
by
A.
corniculatum
and
A.
marina
grown
under
different
salinity
and
humidity
regimes.
'This
work
has
been
submitted
by
M.
C.
B.
in
partial
fulfillment
of
the
requirement
for
the
Ph.D.
degree.
2Abbreviations:
A,
photosynthetic
CO2
assimilation
rate;
c,,
intercel-
lular
CO2
concentration;
A(c,),
assimilation
rate
as
a
function
of
the
intercellular
CO2
concentration;
E,
evaporation
rate;
g,
leaf
(primarily
stomatal)
conductance
to
water
vapor,
vpd,
leaf
to
air
vapor
pressure
difference.
Plant
Material.
Propagules3
of
Aegiceras
corniculatum
(L.)
Blanco
and
Avicennia
marina
(Forstk.)
Vierh.
var
australasica
(Walp.)
Moldenke
were
collected
from
trees
growing
along
Cul-
lendulla
Creek,
New
South
Wales,
Australia
(35°42'S,
150°1
2'E).
These
propagules
were
cultivated
in
sand
beds,
and
subirrigated
with
10%
and
50%
seawater,
respectively,
at
which
growth
of
the
respective
species
is
optimum
at
this
stage
of
their
life
cycle
(1).
The
beds
were
kept
in
a
growth
cabinet
adjusted
to
provide
day/night
leaf
temperatures
of
25/20°C,
RH
of
70%
to
give
a
leaf
to
air
vpd
of
approximately
12
mbar,
and
a
12-h
light
period
with
quantum
flux
density
of
400
uE
m
2
s-'
incident
on
the
bed.
The
propagules
were
kept
in
this
way
for
6
weeks
until
the
cotyledons
had
senesced
and
the
seedlings
had
four
leaves.
Forty-five
seedlings
of
similar
dimensions
and
fresh
weights
were
then
selected
from
the
populations
of each
species
and
divided
into
nine
groups
of
five.
The
seedlings
were
placed
in
plastic
containers
(volume
200
ml
for
A.
corniculatum
and
500
ml
for
A.
marina)
for
hydroponic
culture.
The
seawater
solutions
initially
used
to
cultivate
the
propagules
were
replaced
at
a
rate
of
25%/d
with
Johnson's
nutrient solution
(17)
amended
with
the
appropriate
concentration
of
NaCl
to
maintain
the
salinity.
The
salinities
were
then
adjusted
at
a
rate
of
50
mM
NaCl/d
(approximately
10%
seawater)
to
give
the
three
final
concentra-
tions
of
50,
250,
and
500
mm
NaCl.
Water
levels
were
maintained
by
the
addition
of
demineralized
water
every
other
day
and
solutions
were
changed
weekly.
Seedlings
receiving
these
salinity
treatments
were
then
distrib-
uted
among
three
growth
chambers
adjusted
for
high,
medium,
and
low
humidity
regimes
to
give
a
total
of
nine
growth
condi-
tions.
RH
of
approximately
90,
70,
and
30%
were
used
to
give
vpd
of
6,
12,
and
24
mbar,
respectively.
The
light
period
was
12
h
and
the
average
quantum
flux
density
close
to
the
leaves
was
400
pE
m-2
s-',
as
measured
with
a
Lambda
quantum
sensor.
Day/night
air
temperatures
were
adjusted
to
give
average
leaf
temperatures
of
25/20°C.
The
plants
were
grown
for
3
months
before
gas
exchange
characteristics
were
studied
on
leaves
which
had
developed
fully
under
the
different
salinity
and
humidity
regimes.
The
leaves
had
been
fully
expanded
for
1
week
at
the
time
of
gas
exchange
measurements.
Gas
Exchange.
Rates
of
CO2
and
water
vapor
exchange
in
intact,
attached
leaves
were
determined
with
an
open
system
gas
analysis
apparatus
as
described
by
Wong
et
al.
(30)
with
modi-
fications
as
noted
in
Ball
and
Critchley
(2).
Calculations
are
according
to
von
Caemmerer
and
Farquhar
(29).
The
conditions
of
measurement
were
similar
to
those
in
the
growth
cabinets,
i.e.
3
These
mangroves
are
viviparous
species.
Seeds
germinate
on
the
mother
tree
and
develop
into
seedlings
(propagules),
which
are
the
dispersive
units.

BALL
AND
FARQUHAR
leaf
temperature
of
25°C,
quantum
flux
density
of
500
uE
m-2
s-',
and
vpd
of
6,
12,
or
24
mbar.
Atmospheric
pressure
averaged
950
mbar.
Boundary
layer
conductance
to
water
vapor
was
0.4
mol
m-2
s-'.
Assimilation
rate
was
measured
as
a
function
of
the
intercellular
CO2
concentration,
ci,
by
varying
the
ambient
CO2
concentration
according
to
the
sequence
330,
400,
500,
200,
100,
and
50
,l
I-',
allowing
30
min
at
each
concentration
to
permit
variables
relating
to
gas
exchange
to
attain
steady
state.
All
measurements
were
made
during
normal
photoperiods.
Foliar
Ion
Levels.
Leaves
were
harvested
for
ion
determination
following
measurement
of
their
photosynthetic
characteristics.
Leaves
were
washed
in
distilled
H20,
blotted
dry,
and
weighed
before
oven
drying
at
80°C
to
constant
weight.
The
dry
tissue
was
weighed,
pulverized
in
a
mortar
and
pestle,
and
added
to
double
distilled
H20
(H1
g
tissue/
100
ml
water).
Ions
were
extracted
by
boiling
for
2
h.
The
filtered
extract
was
analyzed
for
Cl-
by
silver
titration
with
a
Buchler-Cotlove
chloridometer
and
for
Na+
and
K+
by
flame
emission
spectroscopy
with
a
Varian
Techtron
Series
AA.6
spectrophotometer.
RESULTS
Ion
Concentrations
in
Leaves.
The
concentrations
of
Cl-,
Na+,
and
K+
in
leaves
of
A.
corniculatum
and
A.
marina
grown
under
different
salinity
and
humidity
conditions
are
summarized
in
Table
I.
Leaves
of
both
species
contained
high
concentrations
of
these
ions
which
accounted
for
as
much
as
4%
to
10%
of
the
total
leaf
dry
weight.
There
was
considerable
variability
in
the
data
within
humidity
treatments,
and
it
appears
that
the
foliar
ion
concentrations
may
be
largely
a
function
of
the
external
salinity.
The
patterns
of
ion
accumulation
differed
between
species
(Table
I).
The
concentrations
of
Cl-
and
Na+
were
maximum
in
leaves
of
A.
corniculatum
grown
in
a
solution
containing
250
mM
NaCl
whereas
those
of
A.
marina
increased
with
increasing
salinity
of
the
growth
media.
The
concentrations
of
Cl-
and
Na+
in
leaves
exceeded
those
of
the
nutrient
solutions
in
which
the
plants
were
grown
except
for
Cl-
in
A.
corniculatum
grown
in
500
mM
NaCl.
Although
growth
of
the
latter
group
of
plants
was
severely
stunted,
they
did
not
show
signs
of
damage.
The
differ-
ence
between
foliar
and
substrate
concentrations
of
Cl-
and
Na+
declined
with
increasing
salinity,
the
differences
being
greater
in
A.
corniculatum
grown
in
50
and
250
mm
NaCl
than
in
A.
marina
grown
under
the
same
conditions.
The
concentration
of
K+
decreased
with
increasing
salinity
in
both
species,
with
A.
marina
maintaining
higher
foliar
levels
of
K+
than
A.
corniculatum
(Table
I).
These
concentrations
are
considerably
greater
than
the
6
mm
K+
in
the
nutrient
solution.
Gas
Exchange
Characteristics
under
Normal
Atmospheric
Conditions,
i.e.
Ambient
CO2
Concentration
of
330
,ul
l`
and
210
ml
Il'
02.
The
gas
exchange
characteristics
of
A.
corniculaturn
and
A.
marina
grown
under
different
salinity
and
humidity
treatments
are
shown
in
Figure
1.
Stomatal
conductance
declined
with
increasing
salinity,
thereby
causing
a
proportional
decrease
in
the
evaporation
rate
because
the
leaf
to
air
vpd
was
maintained
constant
(Fig.
1).
In
A.
corniculatum,
the
decline
in
assimilation
rate
was
relatively
greater
than
the
decrease
in
stomatal
conduct-
ance
with
increasing
salinity.
Thus,
the
assimilation
rate
declined
while
the
intercellular
CO2
concentration
(c1)
increased
(Fig.
1).
In
contrast,
in
A.
marina
the
reduction
in
stomatal
conductance
was
nearly
proportional
to
the
decrease
in
assimilation
rate.
Table
I.
Contents
of
Cl-,
Na+,
and
K+
in
Leaves
of
Aegiceras
corniculatum
and
Avicennia
marina
Grown
under
Different
Salinity
and
vpd
Regimes
Values
are
mean
+
SE,
n
=
S
except
*
in
which
n
=
2.
ND
indicates
no
data;
plants
were
lost
in
an
accident
prior
to
measurements.
Salinity
Humidity
Nae
Species
Nal)
Humdit
Fresh/Dry
Weight
Cl-
Na+
K+
mM
mbar
g
g9'
mmol
ion
kg-'
leaf
water
ratio
A.
corniculatum
50
6
2.71
±0.06
360
±
16
419
±
30
30
±
4
14.87
2.99
12
2.84
±
0.15
343
±
35
465
±
76
70
±
15
8.82
3.50
24
2.77±0.11
416±
14
379±32
68±
10
6.65±0.88
Average
2.77
±0.06
381
±
14
413
±
26
58
±
7
9.49
1.67
250
6
3.69
±
0.12
462
±
8
633
±
4
26
±
3
25.07
2.36
12
3.38
±
0.19
426
±
52
709
±
41
22
±
2
33.78
5.08
24*
3.15±0.35
489±
11
1006±
194
52±8
19.13±0.88
Average
3.41
±
0.10
459
±
15
783
±
98
33
±
4
25.99
2.24
500
6
3.15±0.54
370±
13
514±5
28±7
21.90±5.37
12
3.72±0.06
397±32
571
±33
36±8
21.00±6.13
24
3.26
±
0.23
308
±
17
540
±
34
29
±
3
19.90
3.20
Average
3.42±0.15
356±
17
547
±
17
31
±
3
20.75
2.53
A.
marina
50
6
ND
ND
ND
ND
ND
12
4.00
±
0.67
337
±
38
219
±
27
159
±
25
1.59
±
0.36
24
3.59±0.15
368±34
204±42
157±21
1.31
±0.34
Average
3.80±0.29
352±21
212±
19
157±
13
1.53±0.19
250
6
4.18
±
0.26
482
±
26
398
±
37
67
±
23
6.87
±
1.52
12
3.39
±
0.09
467
±
17
403
±
23
144
±
22
3.09
±
0.47
24
3.66±0.37
490±63
411
±54
97±21
4.46±
1.06
Average
3.67
±0.17
481
±
25
405
±
23
105
±
14
4.50±0.67
500
6
ND
ND
ND ND
ND
12
3.47
±
0.09
534
±
37
409
±
48
91
±
21
5.11
±
0.79
24
3.53±0.11
710±76
611
±94
105
±11
6.18±
1.08
Average
3.50±
0.06
628
±
41
517
±
50
98
±
10
5.68
±
0.55
2
Plant
Physiol.
Vol.
74,
1984

PHOTOSYNTHETIC
RESPONSES
TO
SALINITY
AND
HUMIDITY
250
mM
NaCI
500
mM
NaCI
FIG.
1.
Gas
exchange
characteristics
of
A.
corniculatum
(0)
and
A.
marina
(0)
under
normal
atmospheric
conditions,
i.e.
330
Al
I-'
CO2
and
210
ml
I-'
02.
Values
are
mean
±
SE.
The
values
for
n
are
variable
and
are
listed
in
Table
II.
Leaf
to
air
vapor
pressure
difference
(mbar)
Table
II.
Water
Loss/Carbon
Gain
Ratio
of
A.
corniculatum
and
A.
marina
Grown
under
Different
Salinity
and
Humidity
Regimes
Values
are
mean
mol
H20/mol
CO2
+
SE
(n).
ND
=
no
data.
Species
Humidity
Salinity
(NaCI)
(vpd)
50
250
500
mbar
mM
A.
corniculatum
6
62.5
±
1.4
(5)
71.4
±
5.0
(4)
384.6
±
1.4
(2)
12
135.1
±
5.0
(7)
166.7
±
1.1
(6)
384.6
±
1.4
(2)
24
200.0
±
1.1
(5)
227.3
±
2.0
(3)
ND
A.
marina
6
73.5
±
1.0
(6)
74.1
±
1.4
(4)
80.0
±
1.7
(4)
12
108.7
±
5.0
(7)
119.0
±
5.0
(6)
117.6
±
1.7
(7)
24
181.8
±
10.0
(8)
208.3
±
5.0
(7)
227.3
±
1.7
(8)
Thus,
the
assimilation
rate
declined
while
c,
was
maintained
relatively
constant
with
increase
in
salinity
(Fig.
1).
The
net
effect
of
these
changes
was
that
the
water
loss/carbon
gain
ratio
(EIA)
increased
in
A.
corniculatum
to
a
greater
extent
than
in
A.
marina
with
increase
in
salinity
(Table
II).
Both
the
assimilation
rate
and
stomatal
conductance
decreased
with
increase
in
vpd.
These
changes
were
accompanied
by
a
decline
in
c,
(Fig.
1).
However,
stomatal
closure
in
response
to
increasing
vpd
was
not
sufficient
to
reduce
the
evaporation
rate
and
it
increased
with
increasing
vpd
in
both
species
(Fig.
1).
This
caused
the
EIA
ratio
to
increase
with
increasing
vpd
(Table
II).
Assimilation
Rate
as
a
Function
of
the
Intercellular
CO2
Concentration.
The
photosynthetic
capacity
of
the
mesophyll
can
be
assayed
by
measurement
of
the
assimilation
rate
as
a
function
of
ci,
hereafter
called
the
A(c1)
curve
(10).
Photosynthetic
capacity
declined
with
increasing
salinity,
with
A.
corniculatum
being
the
more
sensitive
species,
as
shown
by
changes
in
the
shapes
of
the
A(c,)
curves.
These
changes
are
exemplified
by
those
shown
in
Figure
2
in
which
it
is
apparent
that
both
the
initial
linear
slope
(Table
III)
and
upper
plateau
of
the
A(c,)
curve
declined
with
increasing
salinity.
Salinity
did
not
affect
the
CO2
compensation
point,
which
averaged
45
±
4
(n
=
34)
and
50
+
4
1-'
(n
=
57)
in
leaves
of
A.
corniculatum
and
A.
marina,
respectively,
grown
under
all
treatments.
Photosynthetic
capacity
also
declined
with
increasing
vpd
as
shown
by
changes
in
the
shapes
of
the
A(ci)
curves
in
Figure
3.
The
assimilation
rate
was
insensitive
to
variation
in
vpd
at
low
ci,
i.e.
there
were
no
effects
on
either
the
CO2
compensation
point
or
the
initial
linear
slope
of
the
A(c,)
curve
(Table
III).
In
contrast,
the
upper
plateau
of
the
A(ci)
curve
was
sensitive
to
50
mM
NaCI
3
07
uo,
c
cl
o
_
E
7_
OC
EE
*0
00
-c
a-
E
0
7s
.2_
O
0
E
-ER
C

BALL
AND
FARQUHAR
0
E
N
0
C)
0
E
7._
.I-
a
n
0
Intercellular
CO2
concentration
(,ul
l-l)
FIG.
2.
Variation
in
the
shapes
of
A(ci)
curves
in
A.
corniculatum
(0,
A,
V)
and
A.
marina
(0,
A,
V)
grown
under
low
vpd
(6
mbar)
and
in
nutrient
solution
containing
50
(0,
0),
250
(A,
A),
and
500
mM
NaCl
(V,
V).
Arrows
indicate
measurements
made
under
normal
atmospheric
conditions.
Data
for
each
set
of
conditions
were
obtained
from
a
single
leaf.
Table
III.
Variation
in
the
Initial
Slope
of
the
A(cJ)
Curves
Determined
in
Leaves
of
A.
corniculatum
and
A.
marina
Grown
under
Different
Conditions
of
Salinity
and
vpd
The
initial
slope
was
calculated
by
linear
regression
of
data
obtained
under
ambient
CO2
concentrations
of
50,
100,
and
200
ol
1-'
from
all
individuals
(n)
receiving
a
particular
combination
of
salinity
and
humid-
ity
treatments.
The
values
for
the
initial
slope
are
given
as
mol
CO2
m-2
s_'
(regression
coefficient).
Values
of
n
are
variable
and
are
listed
in
Table
II.
ND
means
no
data.
Humidity
Salinity
(NaCI)
Species
vd
(vpd)
50
250
500
mbar
mM
A.
corniculatum
6
0.10
(0.96)
0.06
(0.90)
0.02
(0.69)
12
0.10
(0.93)
0.06
(0.88)
0.02
(0.67)
24
0.10
(0.92)
0.08
(0.83)
ND
A.
marina
6
0.14
(0.87)
0.09
(0.98)
0.08
(0.95)
12
0.13
(0.93)
0.10
(0.94)
0.07
(0.85)
24
0.14
(0.90)
0.10
(0.92)
0.08
(0.74)
vpd.
Curvature
from
the
initial
linear
slope
began
at
lower
ci
with
increasing
vpd
such
that
the
assimilation
rate
declined
at
high
ci.
DISCUSSION
Growth
of
Aegiceras
corniculatum
is
more
sensitive
to
salinity
than
that
of
a
sympatric
species,
Avicennia
marina
(1).
The
former
species
also
showed
a
greater
increase
in
the
ratio
of
water
loss
to
carbon
gain
than
the
latter
with
increase
in
either
the
salinity
or
vpd
in
which
the
plants
were
grown
(Table
II).
These
transpiration
ratios
are
the
outcome
of
changes
in
gas
exchange
characteristics,
but
give
an
incomplete
picture
of
the
effectiveness
of
water
use
in
relation
to
carbon
gain.
This
is
best
understood
by
examination
of
stomatal
functioning
with
respect
to
the
2
E
0
E
0
0
0
0
c
.8
n
50
100
150
200
250
Intercellular
CO2
concentration
(pi.
1I1)
FIG.
3.
Variation
in
the
shapes
of
A(c,)
curves
in
A.
cornictilattim
(0,
A,
V)
and
A.
marina
(0,
A,
V)
grown
in
nutrient
solution
containing
50
mM
NaCl
and
under
a
vpd
of
6
(0,
0),
12
(A,
A),
and
24
mbar
(V,
V).
Arrows
indicate
measurements
made
under
normal
atmospheric
condi-
tions.
Data
for
each
set
of
conditions
were
obtained
from
a
single
leaf.
photosynthetic
capacity
of
the
mesophyll.
Responses
of
Photosynthesis
to
Salinity.
In
the
present
study,
the
photosynthetic
capacities
of
A.
corniculatum
and
A.
marina,
both
C3
species,
declined
with
increasing
salinity
as
shown
by
changes
in
the
shapes
of
the
A(ci)
curves
(Fig.
2).
One
component
of
the
decrease
in
photosynthetic
capacity
was
a
decline
in
the
initial
linear
slope
of
the
A(ci)
curve
with
increasing
salinity
(Table
III)
consistent
with
earlier
reports
on
glycophytes
(10,
12,
18)
and
halophytes
(8,
14,
18,
19)
grown
in
sub-
or
supra-optimal
salinities.
Another
component,
which
has
not
been
studied
pre-
viously,
was
a
decline
in
the
level
of
the
upper
plateau
of
the
A(c,)
curve
with
increasing
salinity
(Fig.
2),
indicating
an
increase
in
intrinsic
limitation
to
the
CO2
assimilation
rate
at
high
CO,
concentrations.
Leaves
of
A.
corniculatum
and
A.
marina
accumulated
high
levels
of
inorganic
ions
which
were
more
than
sufficient
to
maintain
leaf
osmotic
pressures
at
higher
levels
than
those
of
the
saline
conditions
experienced
at
the
roots
(Table
I),
similar
to
the
results
of
previous
studies
with
A.
marina
(9).
Despite
these
high
concentrations
of
ions
in
the
leaves,
the
changes
in
gas
exchange
characteristics
with
increasing
salinity
(Fig.
2)
are
sim-
ilar
to
those
observed
in
glycophytes
in
response
to
long
term
water
stress,
e.g.
those
obtained
by
exposing
plants
to
fixed
osmotic
pressures
during
growth
or
by
allowing
plants
to
gradu-
ally
deplete
the
soil
water
content
of
a
pot.
For
example,
similar
changes
in
the
shapes
of
A(c,)
curves
were
observed
in
Eucalvptuts
socialis
(6),
Larrea
divaricata
(20),
and
Simmondsia
chinensis
(5)
with
gradual
imposition
of
water
stress.
Few
other
workers
have
reported
measurements
of
A(c1)
curves,
but
similar
effects
to
the
decrease
in
the
initial
slope
are
evident
from
calculated
increases
in
mesophyll
resistance
with
increasing
water
stress
in
several
species
(4,
22,
23).
The
similarity
in
these
responses
suggests
that
changes
in
leaf
water
relations
associated
with
the
salinity
conditions
experienced
during
growth
may
have
directly
or
indirectly
influenced
photosynthetic
metabolism.
Other
observations
suggest
that
the
decline
in
photosynthetic
:
v
A.
cornicla/otum
o
4/
'5-
I~~~~~~~~~~~~
I0
I~~~~~~~~
5
0
!O-A.
marina
0--
10~~~~~~~~~
5-
4
Plant
Physiol.
Vol.
74,
1984
,^
2

PHOTOSYNTHETIC
RESPONSES
TO
SAL!NITY
AND
HUMIDITY
capacity
with
increasing
salinity
may
be
related
to
internal
ion
concentrations,
particularly
the
Na+
to
K+
ratio.
It
increased
with
increasing
salinity
(Table
I),
presumably
because
the
high
levels
of
Na+
present
in
culture
solutions
interfered
with
K+
absorption
(16,
21, 25,
26).
It
should
be
noted
that
the
K+
concentration
in
the
nutrient
solutions
was
6
mm,
whereas
open
seawater
typically
contains
10
mm
K+.
Further,
the
Na+
to
K+
ratio
at
the
roots
would
remain
constant
in
dilutions
of
seawater,
whereas
the
ratio
varied
as
the
Na+
level
increased
from
50
to
500
mM
in
the
nutrient
solutions
of
the
present
study.
The
decline
in
the
K+
concentration
in
the
leaves
(Table
I)
was
accompanied
by
decrease
in
the
initial
slope
of
the
A(ci)
curve
(Fig.
2;
Table
III),
which
can
be
a
symptom
of
K+
defi-
ciency
(24,
27,
28).
A.
corniculatum
apparently
has
a
lower
selectivity
for
K+
absorption
under
saline
conditions
than
A.
mnarina
(Table
I)
and
the
decline
in
the
initial
slope
of
the
A(c,)
curve
was
greater
in
the
former
than
in
the
latter
species
with
increasing
salinity
(Table
III).
Conversely,
the
photosynthetic
capacity
of
A.
marina
was
unaffected
by
the
same
range
of
salinity
(1)
when
the
plants
were
grown
such
that
the
K+
concen-
tration
of
the
leaves
increased
with
increasing
salinity.
It
is
possible
that
A.
corniculatum
and
A.
marina
may
have
experi-
enced
some
metabolic
dysfunction
relating
to
their
requirements
for
K+
and
the
capacity
to
satisfy
those
needs
with
increasing
salinity.
Responses
of
Photosynthesis
to
Humidity.
The
decline
in
photosynthetic
capacity
with
increasing
salinity
was
enhanced
by
increasing
vpd.
In
contrast
to
the
aforementioned
effects
of
salinity,
the
decrease
in
photosynthetic
capacity
with
decrease
in
humidity
was
due
only
to
a
decline
in
the
level
of
the
upper
plateau
of
the
A(c,)
curve
(Fig.
3).
No
comparable
data
from
long
term
treatments
are
available.
However,
it
has
been
shown
in
a
subsequent
study
on
A.
marina
(1)
that
exposure
to
short
term
(i.e.
2
h
and
2
d)
changes
in
vpd,
or
more
specifically
in
the
transpiration
rate,
caused
reversible
effects
in
the
plateau
region
of
the
A(c,)
curve
similar
in
magnitude
to
those
reported
here.
Thus,
there
may
have
been
little
intrinsic
effect
of
vpd
experi-
enced
during
growth
on
the
A(c1)
characteristics.
Integration
of
the
Responses
of
Photosynthesis
and
Stomatal
Conductance
to
Variation
in
Salinity
and
Humidity.
Stomata,
through
their
influence
on
ci,
may
modify
the
assimilation
rate
under
normal
atmospheric
conditions.
This
influence
of
stomatal
conductance
is
shown
by
examining
the
shape
of
the
A(c1)
curve
with
reference
to
the
operational
point
at
which
the
leaf
normally
functions,
i.e.
the
point
corresponding
to
an
ambient
CO2
con-
centration
of
330
,g
I-'.
These
operational
points
are
summarized
1.5
A.
cornicul/tum
.
A.
marina
0
0.5
1.0
1.5
2.0
0
0.5
1.0
1.5
(ci
-r
)1(Cj.-r)
FIG.
4.
Normalization
of
A(c,)
curves
measured
in
A.
corniculatum
and
A.
marina
grown
under
all
salinity
and
humidity
treatments
to
emphasize
the
position
of
the
operational
c,
relative
to
the
shape
of
the
A(c,)
curve.
The
assimilation
rate,
A,
is
expressed
relative
to
AO
and
c,
-
F
is
expressed
relative
to
ci0
-
F
where
r
is
the
CO2
compensation
point
and
(c,0,
AO)
is
the
operational
point,
i.e.
the
characteristics
obtaining
under
normal
atmospheric
conditions
with
an
ambient
CO2
concentra-
tion
of
330
,ul
1-'.
The
operational
points
thus
coincide
at
(1,1)
and
are
indicated
by
arrows.
Lines
are
drawn
by
eye.
I
.
N
E
0.
0
_
0.
I-
C
I
0
0
o
0
w
0.
0.
5
5
10
15
20
Assimilation
rate
(
.tmolm-2s-1
)
FIG.
5.
Relationship
between
evaporation
rate
and
assimilation
rate
if
stomatal
conductance
were
to
vary
independently
in
A.
cornicullatulm
and
A.
marina
grown
at
salinities
of
(A)
50,
(B)
250,
and
(C)
500
mM
NaCI.
Calculations
were
made
from
the
A(c,)
data
presented
in
Figure
2
and
are
discussed
in
the
text.
Arrows
indicate
the
values
measured
under
normal
atmospheric
conditions.
0
E
-
E
E
0
0
0
w
u
5
10
I5
20
Assimilation
rate
(,Lrmolm
2s-1
)
FIG.
6.
Relationship
between
evaporation
rate
and
assimilation
rate
if
stomatal
conductance
were
to
vary
independently
in
A.
cornicullatulm
and
A.
marina
grown
with
a
leaf
to
air
vapor
pressure
difference
of
(A)
6,
(B)
12,
and
(C)
24
mbar.
Calculations
were
made
from
the
A(cj)
data
presented
in
Figure
3
as
discussed
in
the
text.
Arrows
indicate
the
values
measured
under
normal
atmospheric
conditions.
in
Figure
1,
but
the
significance
in
relation
to
the
shape
of
the
A(c,)
curves
is
presented
more
clearly
in
Figure
4.
It
is
apparent
that
the
variation
in
stomatal
conductance
(Fig.
1)
was
such
that
the
operational
c,
(Fig.
1)
occurred
near
the
region
of
transition
between
the
lower
linear,
and
upper
plateau
portions
of
the
A(c,)
curves
in
all
treatments
(Fig.
4).
This
shows
that
stomatal
con-
ductance
and
photosynthetic
capacity
change
in
the
same
sense
and
therefore
co-limit
the
assimilation
rate
as
discussed
in
the
accompanying
paper
(3).
s
_
A.
cornicula/tum
c
C
'
'B
I'
5-
A.
marina
5
:
C
B
I'A
I
5
-
o
I_
I_
A.
corniculatum
;
5
4
c
3
-I
-C
A
A.
marina
5
-:
4
3
-I
2
_
I,
+
B
I
_
A
'
b
v.
w

6.
BALL
AND
FARQUHAR
The
occurrence
of
the
operational
c1
in
the
transition
region
of
the
A(c,)
curve
has
implications
for
water
loss
in
relation
to
carbon
gain
as
shown
in
Figures
5
and
6.
These
graphs
show
the
simultaneous
changes
in
the
rates
of
evaporation
and
assimila-
tion
of
plants
grown
under
different
salinity
and
humidity
con-
ditions,
respectively,
which
would
occur
if
stomatal
conductance
were
the
independent
variable.
These
curves
were
calculated
according
to
Farquhar
and
Sharkey
(11),
assuming
that
leaf
temperature
remained
constant
and
ignoring
the
effects
of
changes
in
the
transpiration
rate
on
the
assimilation
rate
(1).
Thus,
the
values
of
the
assimilation
rate
corresponding
to
the
plateau
region
of
the
A(c1)
curve
are
overestimated
in
Figures
5
and
6,
and
the
lines
are
dashed
to
emphasize
this
uncertainty.
With
c;
occurring
in
the
transition
region
of
the
A(c,)
curve,
further
opening
of
the
stomata
leading
to
an
increase
in
c,
would
cause
an
increase
in
the
assimilation
rate
which
is
less
than
proportional
to
the
increase
in
c;,
whereas
closure
would
cause
a
decrease
which
is
proportional.
Thus,
the
sensitivity
of
the
assim-
ilation
rate
to
change
in
the
stomatal
conductance
to
water
vapor,
dA/Og,
shows
large
changes
in
the
transition
region
of
the
A(c1)
curve.
In
contrast,
the
evaporation
rate
varies
directly
with
stomatal
conductance
provided
that
the
boundary
layer
con-
ductance
is
comparatively
large.
Thus,
the
sensitivity
of
the
evaporation
rate
to
change
in
stomatal
conductance,
E/Og,
shows
little
change
over
the
same
region
of
the
A(c,)
curve.
This
causes
the
ratio
of
these
two
sensitivities,
dE/dA
or
the
marginal
water
cost
of
carbon
assimilation
(7),
to
show
large
changes
in
the
transition
region
of
the
A(c1)
curve
(3,
29).
It
is
evident
that
there
can
be
a
large
range
of
values
of
OE/6A
for
which
minimal
water
loss
relative
to
carbon
gain
requires
the
operational
c,
to
be
in
the
transition
region
of
the
A(ci)
curve
(3,
29)
as
occurred
in
the
present
study
under
all
treatments
(Fig.
4).
The
values
of
dPEIA
at
the
operational
points
in
Figures
5
and
6
and
in
other
data
not
shown
were
approximately
250
mol
H20/mol
CO2.
In
summary,
there
were
substantial
differences
in
both
the
way
in
which
photosynthetic
metabolism
changed
with
variation
in
salinity
and
humidity
conditions
and
in
the
extent
to
which
photosynthesis
of
A.
corniculatum
and
A.
marina
was
sensitive
to
these
treatments
(Figs.
2
and
3).
Despite
these
differences,
stomatal
behavior
was
such
that
the
operational
ci
occurred
in
the
transition
region
of
the
A(c,)
curve
(Fig.
4).
This
behavior
has
two
major
consequences
to
the
carbon
and
water
economy
of
the
leaf.
First,
the
facility
with
which
CO2
was
allowed
to
enter
the
leaf
was
consistent
with
the
capacity
of
the
leaf
to
assimilate
CO2
under
all
treatments
(Figs.
2-4).
Second,
water
loss
was
minimum
relative
to
carbon
gain
(Figs.
5
and
6)
even
though
differences
in
the
proportionality
between
stomatal
conductance
to
water
vapor
and
photosynthetic
CO2
assimilation
(Fig.
1)
caused
the
transpiration
ratio,
E/A,
to
vary
(Table
II).
Acknowledgments-It
is
a
pleasure
to
thank
Professor
C.
Barry
Osmond
and
Drs.
Eldon
Ball,
Ian
Cowan,
and
Thomas
Sharkey
for their
thoughtful
comments
and
criticisms
during
this
study,
and
Dr.
S.
C.
Wong
and
Mr.
Win
Coupland
for
technical
expertise.
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