Download Photosynthetic responses to water deficit in six

Tree Physiology 22, 687–697
© 2002 Heron Publishing—Victoria, Canada
Photosynthetic responses to water deficit in six Mediterranean
sclerophyll species: possible factors explaining the declining
distribution of Rhamnus ludovici-salvatoris, an endemic Balearic
species
J. GULÍAS,1 J. FLEXAS,1,2 A. ABADÍA3 and H. MEDRANO1
1
Laboratori de Fisiologia Vegetal, Departament de Biologia, Universitat de les Illes Balears, Carretera de Valldemossa, Km. 7.5, 07071 Palma de
Mallorca, Balears, Spain
2
Author to whom correspondence should be addressed ([email protected])
3
Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei (Consejo Superior de Investigaciones Científicas), Apartado 202, 50080
Zaragoza, Aragón, Spain
Received September 25, 2001; accepted December 31, 2001; published online June 3, 2002
Summary We sought to explain the declining distribution in
the Balearic Islands of the endemic shrub Rhamnus ludovicisalvatoris R. Chodat, by comparing its photosynthetic response to drought with that of several widely distributed, competing Mediterranean species (R. alaternus L., Quercus ilex L.,
Pistacia lentiscus L., Q. humilis Mill. and P. terebinthus L.).
All of the study species, except for the two Rhamnus species, avoided desiccation by rapidly adjusting their stomatal
conductance at the onset of drought, and maintaining constant
leaf relative water content. The two Rhamnus species showed
desiccation-tolerant behavior; i.e., as drought progressed,
their predawn leaf relative water content decreased simultaneously with stomatal closure. All four desiccation-avoiding
species showed a significant positive correlation between leaf
thermal dissipation (estimated by the fluorescence parameter
NPQ (non-photochemical quenching)) and the de-epoxidation
state of the xanthophyll cycle (DPS). The two Rhamnus species exhibited maximum DPS regardless of treatment, but
only R. alaternus increased NPQ in response to drought.
Rhamnus ludovici-salvatoris had a high ratio of photorespiration to photosynthesis and a low intrinsic water-use efficiency; traits that are likely to be unfavorable for plant productivity under arid conditions. It also had the lowest DPS and
thermal dissipation among the six species. We conclude that
the photosynthetic traits of R. ludovici-salvatoris account for
its limited ability to compete with other species in the Mediterranean region.
Keywords: chlorophyll fluorescence, deciduous, drought, evergreen, gas exchange, leaf mass area, nitrogen, Pistacia,
Quercus, Rhamnus, xanthophyll cycle.
Introduction
Drought is the main environmental constraint on plant biomass production in the Mediterranean region. Consequently, it
is likely that ecophysiological traits that determine the ability
of a species to cope with drought partially explains its distribution and ecological fitness in the Mediterranean region (Bazzaz 1979, Schulze 1982, Lambers et al. 1998). The intrinsic
link between photosynthesis and biomass production suggests
that photosynthesis and its response to drought is likely to play
a major role in determining the ability of tree seedlings to establish in drought-prone areas, because unlike adult trees,
seedlings do not possess additional compensatory mechanisms such as deep roots or dense canopies. The closest association between leaf photosynthesis and plant growth is seen
in young plants, a fact attributable to their low leaf area index
(Gardner et al. 1985). A good correlation between net photosynthesis and relative growth rate has been observed in saplings (Pattison et al. 2001) and a correlation between seasonal
photosynthesis and the percentage of ground covered was
found in Chaparral species (Oechel et al. 1981).
Differences in photosynthetic properties and responses to
drought between evergreen and winter deciduous species may
account for differences in the distribution patterns of the two
groups of species in Mediterranean-type ecosystems (Ehleringer and Mooney 1982, Ne’eman and Goubitz 2000). Deciduous species generally predominate in cold and humid subMediterranean regions and compensate for their shorter
growth period with a higher photosynthetic capacity (Ehleringer and Mooney 1982, Ne’eman and Goubitz 2000, but see
Damesin et al. 1998). In contrast, evergreen species predominate in the hot and dry Mediterranean regions, where they can
maintain high photosynthetic rates during winter when deciduous species are photosynthetically inactive.
Endemic plants account for 7–8% of the flora of the Mediterranean islands (Cardona and Contandriopoulos 1979).
However, judging from their declining distribution and high
extinction rates (Alomar et al. 1997), some endemic species
are poorly adapted to present conditions. Because climate
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GULÍAS, FLEXAS, ABADÍA AND MEDRANO
change models predict that more arid conditions will prevail in
the Mediterranean Basin (Osborne et al. 2000), many of these
species may become extinct. A recent survey of Balearic endemic species showed that these plants have a lower photosynthetic capacity under optimal conditions than their widespread
relatives (J. Gulías et al., unpublished results). The low photosynthetic capacity was associated with low specific leaf area
and photosynthetic nitrogen-use efficiency.
We studied Rhamnus ludovici-salvatoris R. Chodat, an endemic evergreen shrub that declined in distribution during the
last century. Until recently, this species was found in Cabrera,
Menorca, Serra de Tramuntana and Serra de Llevant (the last
two areas located on the island of Mallorca) (Alomar et al.
1997). Today, however, the species has disappeared from
Menorca and Serra de Llevant. Furthermore, where it survives, the populations are characterized by a low proportion of
seedlings and young saplings, suggesting low establishment
success. The main objective of this study was to compare the
photosynthetic response to drought of saplings of R. ludovicisalvatoris with that of species that are widely distributed in the
Mediterranean region. A second goal was to evaluate whether
other species with low distribution in the Balearic Islands (i.e.,
winter deciduous species) have the same leaf traits as R. ludovici-salvatoris.
the shrubs (P. lentiscus and the two Rhamnus species) are
nanophylls, and the trees (P. terebinthus and the two Quercus
species) are nano-microphylls or microphylls (Christodoulakis and Mitrakos 1987). All these species share some basic
characteristics: they have a Mediterranean origin and distribution (Suc 1984, Castro-Díez et al. 1998, Ne’eman and Goubitz
2000), they are currently growing within the Mediterranean
oak forests and related successional communities (Tomaselli
1981, Suc 1984), and they are sclerophyllous (Christodoulakis
and Mitrakos 1987).
The study plants, six per species, were grown outdoors at
the University of the Balearic Islands (Mallorca, Spain), in
large pots (volume 60 l, height 60 cm) containing a 1:1 (v/v)
mixture of clay–calcareous soil and horticultural substrate.
Although the pots may eventually limit root growth, they otherwise simulate natural conditions because about 85% of root
biomass of sclerophyllous shrubs is located in the upper 50 cm
of the soil profile (Jackson et al. 1996). The plants were
5 years old at the onset of the experiments, which were conducted during the summers (July–September) of 1998, 1999
and 2000. The environmental conditions during these summers were similar, with a mean maximum temperature of
30 °C and a mean minimum temperature of 19 °C, no rain and
a mean monthly evapotranspiration of 160 l m –2.
Materials and methods
Treatments and water status determination
Plant material and environmental conditions
Mallorca, the largest Balearic Island, is situated in the western
Mediterranean Basin (39°15′ to 40°00′ N, 2°15′ to 3°30′ E).
The climate is Mediterranean, with a mean annual rainfall
ranging from 300 mm on the south coast to more than
1000 mm in some mountain areas in the northwest. Rain falls
mainly from September to April, and drought can last for
5–6 months. The dominant vegetation comprises evergreen
sclerophyll shrublands (dominated by Pistacia lentiscus L.,
Rhamnus alaternus L. and Olea europaea L.) and woodlands
(dominated by the holm oak, Quercus ilex L.). Winter deciduous woodlands are absent.
Six species were studied: Rhamnus alaternus, R. ludovicisalvatoris, Quercus ilex, Q. humilis Mill., Pistacia lentiscus
and P. terebinthus L. Rhamnus alaternus, P. lentiscus and
Q. ilex are evergreen plants (two shrubs and a tree, respectively) widely distributed on the Balearic Islands and along the
western Mediterranean Basin. Rhamnus ludovici-salvatoris is
an evergreen shrub of limited distribution, endemic to the
Balearic Islands. Its distribution has diminished during the last
century, with the extinction of several populations (authors’
unpublished observations). At present, this species is present
in only certain localities of Mallorca and Cabrera, a small island south of Mallorca. Pistacia terebinthus and Q. humilis are
winter deciduous trees (the former frequently appearing as a
shrub), typical of Mediterranean conditions wetter than those
in Mallorca. The distribution area of P. terebinthus in Mallorca is limited to some humid mountain areas, whereas
Q. humilis is absent from the Balearics. Among these species,
Mid-morning (i.e., maximum) light-saturated stomatal conductance (g) is very sensitive to water stress. Its complex regulation depends on interactions with soil water status, xylem
abscisic acid (ABA) content, leaf water status and other factors. We have recently shown that g is indicative of leaf water
stress, regardless of the factor causing the stress (Flexas et al.
2002, Medrano et al. 2002). Our main rationale for using g as
an indicator of water stress is that many species (including
those studied here) have similar reductions in photosynthesis
at any given g, irrespective of leaf water status and leaf-to-air
vapor pressure deficit (Medrano et al. 2002). Based on this criterion, mild drought treatments and severe drought treatments
were defined as soil water deficits causing 50 and 75% reductions in maximum g (i.e., relative to the control treatment), respectively. The drought treatments were imposed by withholding water, and mid-morning g values were measured daily
until the values corresponding to each treatment were reached.
Typically, under summer conditions, water was withheld for
about 3 days to achieve a mild drought and for 4–6 days to
achieve a severe drought.
Although mid-morning g values were used to define the
drought treatments, two other independent measurements
were also performed to characterize the degree of drought
exposure. First, soil water content was determined in four to
eight randomly chosen pots per treatment by time domain
reflectometry (TDR, Trime System, Imko, Ettlingen, Germany), and referred to as percent of field capacity. Soil water
content was 100% (by definition) under well-watered conditions (control), 84 ± 3% for mild drought and 42 ± 2% for severe drought. Second, six leaves per species and treatment
TREE PHYSIOLOGY VOLUME 22, 2002
DROUGHT AND PHOTOSYNTHESIS IN MEDITERRANEAN SPECIES
were sampled before sunrise to determine relative water content (RWC = (fresh weight – dry weight)/(turgid weight – dry
weight)). The turgid weight of the leaves was determined after
24 h in distilled water at 4 °C in the dark. Dry weights were obtained after oven-drying for 48 h at 70 °C.
Determination of leaf mass area and leaf nitrogen
Samples of the leaves that were used for gas exchange measurements were analyzed for leaf nitrogen concentration ([N])
with an elemental analyzer (Model EA 1108, Carlo Erba Instruments, Milan, Italy). Leaf mass area (LMA = leaf dry
weight/fresh leaf area) was determined with an AM-100 leaf
area meter (ADC, Herts, U.K.), after which the leaves were
dried and weighed.
Gas exchange measurements
Gas exchange measurements were determined on attached
fully expanded leaves in saturating light (1000 µmol m –2 s –1)
with a portable IRGA (LI-6400, Li-Cor, Lincoln, NE). When
four to six sun-exposed leaves of a given plant showed a g
value corresponding to the desired treatment (see above), two
were chosen to construct a light- and a CO2-response curve,
respectively. This selection procedure was repeated for four
replicates per treatment. Temperature was maintained at 30 °C
with a relative humidity of 40–60% inside the leaf chamber
during measurements (leaf temperatures were between 28 and
33 °C, and leaf-to-vapor pressure deficits were between 2 and
3 kPa). These measurements were completed during the morning to avoid the midday depression of photosynthesis and
stomatal conductance.
The LI-6400 light source enabled automatic changes in photosynthetic photon flux density (PPFD), which were applied at
3–5 min intervals to determine the light response curves. The
PPFDs were 1500, 1000, 750, 500, 200, 50, 25 and 0 µmol m –2
s –1. The CO2 flux was adjusted to maintain a concentration inside the chamber of 360 µmol mol –1.
The CO2 response curves were determined at a PPFD of
1000 µmol m –2 s –1. The different CO2 concentrations were obtained from portable CO2/air mixture tanks and automatically
controlled by the LI-6400 CO2 injector. The CO2 concentration ([CO2]) was first set near zero and then progressively increased to 50, 100, 200, 360, 500, 650 and 800 µmol mol –1
(Escalona et al. 1999). Gas exchange measurements were determined at each step after maintaining the leaf at the new
[CO2] for 5 min. The sub-stomatal [CO2] (Ci) was calculated
according to von Caemmerer and Farquhar (1981).
The net CO2 assimilation (AN) versus PPFD and AN versus
Ci curves were fitted with Sigma Plot 4.0 for Windows (SPSS)
by nonlinear regression to hyperbolic and exponential equations, respectively (Martin and Ruiz-Torres 1992, Escalona et
al. 1999). Apparent quantum yield (φ) and apparent carboxylation efficiency (ε) were estimated as the initial slopes of the
AN –PPFD and AN –Ci curves, respectively. The compensation
points for light (k) and CO2 (Γ) were calculated from the x-intercepts of the AN –PPFD and AN –Ci curves, respectively.
Dark respiration (RD) was measured after holding the leaves in
689
darkness. The stomatal limitation to photosynthesis (l) was
calculated from AN –Ci curves according to Farquhar and
Sharkey (1982).
Maximum photosynthetic rates at saturating light and [CO2]
(Amax) were not measured during construction of the AN –Ci
curves, because the [CO2] was not increased above 800 µmol
mol –1 to avoid any interference of high [CO2] with stomatal
conductance. To ensure that Amax values estimated by the exponential adjustments were close to the real Amax values, we
applied higher CO2 concentrations to different leaves than
those used for the construction of the AN –Ci curves. These
leaves were clamped in the LI-6400 chamber at atmospheric
[CO2] and allowed to stabilize. The [CO2] was then immediately (within 1 min) increased to 2000 µmol mol –1, and
stomatal conductance monitored continuously. After about
1 min, photosynthesis was stable, and g was almost unchanged. The value of Amax was then recorded. Figure 1 shows
the relationship between the measured Amax and that estimated
from exponential adjustments. All values fall near the 1:1 ratio, indicating that the estimated values of Amax are reasonable.
Extrapolation of the curve to Ci = 0 (R L) was used to estimate the sum of photorespiration and mitochondrial respiration in the light. Although this method could overestimate
actual photorespiration, the range of values obtained was consistent with estimations made according to the model of Valentini et al. (1995), which is based on combining gas exchange
and chlorophyll fluorescence measurements (data not shown).
Chlorophyll fluorescence measurements
Chlorophyll fluorescence parameters were measured on attached leaves. For each treatment, six measurements were
made on six leaves (i.e., two leaves per plant) with a portable
pulse amplitude modulation fluorometer (PAM-2000, Walz,
Effeltrich, Germany). At predawn (0600 h), the background
Figure 1. Relationship between light- and CO2-saturated photosynthetic rate (Amax) measured at 2000 µmol CO2 mol –1 and that estimated from exponential adjustments of AN versus C i curves.
Abbreviations: R.l-s. = Rhamnus ludovici-salvatoris; R.a. = Rhamnus
alaternus; Q.i. = Quercus ilex; Q.h. = Quercus humilis; P.l. = Pistacia
lentiscus; and P.t. = Pistacia terebinthus.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
690
GULÍAS, FLEXAS, ABADÍA AND MEDRANO
fluorescence signal (Fo), the maximum fluorescence (Fm) and
the maximum quantum yield of photosystem II (PSII) (Fv /Fm
= (Fm – Fo)/Fm) were determined at an irradiance of 0.5 µmol
m –2 s –1 and a frequency of 600 Hz. Steady-state fluorescence
(Fs) in mid-morning sunlight was determined at an irradiance
of 0.5 µmol m –2 s –1 and a frequency of 20 kHz. The PPFD incident on the leaves was always higher than 1000 µmol m –2 s –1,
which was above photosynthesis saturation in these plants. To
obtain the steady-state maximum fluorescence yield (Fm′),
saturation pulses of about 10,000 µmol m –2 s –1 and 0.8-s duration were applied. The PSII photochemical efficiency
(∆F/Fm′) was then calculated according to Genty et al. (1989):
∆F/ Fm′ = ( Fm′ − Fs ) / Fm′,
(1)
and used to determine the linear electron transport rate (ETR)
(Krall and Edwards 1992):
ETR = ( ∆F / Fm′ PPFD0.5 ) 0.84,
(2)
where PPFD is photosynthetic photon flux density incident on
the leaf, 0.5 is a factor that assumes an equal distribution of energy between the two photosystems, and 0.84 is the leaf absorptance for many sclerophyll species (Ehleringer and
Comstock 1987). In this study, leaf absorptance was estimated
according to Sharp et al. (1984). No significant differences
were observed among the six species (data not shown). Nonphotochemical quenching of chlorophyll fluorescence (NPQ)
at mid-morning was calculated as:
NPQ = ( Fm − Fm′ ) / Fm′.
(3)
Pigment analyses
Immediately after chlorophyll fluorescence measurements (at
predawn and midday), discs were punched from leaves of the
same plants showing the same orientation as those used for
fluorescence measurements and submersed in liquid nitrogen.
Six samples per treatment were taken from different plants
(around three to four leaves per sample). The values presented
are means ± SE. Pigments were extracted by grinding leaf tissue in a mortar with acetone (1 cm2 of leaf tissue per ml of solvent) in the presence of sodium ascorbate. Pigments were
identified and quantified by high performance liquid chromatography according to Abadía and Abadía (1993).
Statistical analyses
Statistical analyses of the data were performed with the SPSS
9.0 software package (SPSS, Chicago, IL). Pearson’s correlation analysis was performed on all the studied parameters.
Two-way ANOVAs, with treatment and species as factors,
were performed for the studied parameters. Differences between means were revealed by Tukey’s highest significant difference (HSD) analyses (P < 0.05).
Results
Maximum photosynthesis and stomatal conductance values
Maximum values of photosynthesis and stomatal conductance
(Table 1) of the experimental plants were similar to those obtained for the same species under field conditions. Net photosynthetic rates were about 15–16 µmol m –2 s –1 for the Quercus
species and for P. terebinthus (see Gucci et al. 1997, Damesin
et al. 1998, Gulías et al. 2002), and about 11 µmol m –2 s –1 for
the Rhamnus species and for P. lentiscus (see Gucci et al.
1997, Flexas et al. 2001, J. Gulías et al., unpublished results).
The values under mild and severe drought were similar to
those of field-grown plants at the beginning and at the end of
the summer, respectively (Damesin and Rambal 1995, GarcíaPlazaola et al. 1997, Faria et al. 1998, Flexas et al. 2001,
Gulías et al. 2002).
Variations in RWC, LMA and leaf N concentration with
declining g
A summary of the ANOVA of the effects of drought treatment
and species, and the combined treatment × species interaction
on mid-morning g, predawn leaf relative water content
(RWC), leaf mass area (LMA) and leaf [N] is shown in Table 2. Drought treatment had little effect on RWC; that is, g
was reduced by half before any change in RWC could be detected. However, the highly significant effect of the combined
treatment × species interaction reveals species-dependent differences in the RWC response. As shown in Figure 2, the
Quercus and Pistacia species showed changes in RWC of less
than 10%, even when stomatal closure was pronounced (we
therefore refer to these species as desiccation avoiders). In
contrast, both Rhamnus species showed large reductions in
RWC (> 10%) in response to soil water depletion that were
paralleled by stomatal closure (a response characteristic of
desiccation-tolerant species). A small reduction in RWC in response to severe drought has been reported in some species
(Henson et al. 1989), and may be a result of tight stomatal regulation in response to rapidly imposed drought.
Drought did not significantly affect LMA. The highly significant effect of the treatment × species interaction on LMA
was caused by the two Rhamnus species, which showed progressively increasing LMA with increasing soil water depletion. Because leaf growth was complete before the start of the
experiments, it is likely that the observed treatment effect on
LMA was simply a result of interannual differences.
Although there were significant effects of treatment, species and treatment × species interaction on leaf [N], the treatment effect was evident only under severe drought. Even
under severe drought, leaf [N] was reduced by less than 30%
(Table 2), whereas g was reduced by 75%, suggesting that the
reduction in leaf [N] was a consequence of low water uptake
by roots as a result of reduced transpiration. Because no leaf or
shoot growth was observed during the experiment, we assumed that any influence of developmental and nutritional differences between treatments was low.
TREE PHYSIOLOGY VOLUME 22, 2002
DROUGHT AND PHOTOSYNTHESIS IN MEDITERRANEAN SPECIES
691
Table 1. Mean values for the study species and treatments of most of the parameters studied. Different letters indicate significantly (P < 0.05) different means among treatments and species (that is a total of 18 treatments, these being the 18 species × treatment combinations). Abbreviations: g
(mmol H2O m –2 s –1) = stomatal conductance; RWC (%) = relative water content; LMA (g m –2) = leaf mass area; [N] (mg g –1 dry weight) = leaf
nitrogen concentration; AN (µmol m –2 s –1) = net CO2 assimilation; A/g (µmol mol –1) = intrinsic water-use efficiency; φ (mol quantum –1) = apparent quantum yield; k (µmol m –2 s –1) = compensation points for light; RD (µmol m –2 s –1) = dark respiration ; Amax (µmol CO2 m –2 s –1) = light- and
CO2-saturated photosynthesis; ε (mol –1) = apparent carboxylation efficiency; Γ (µmol mol –1) = compensation point for CO2; RL (µmol m –2 s –1) =
the sum of photorespiration and mitochondrial respiration in the light; l (dimensionless) = stomatal limitation to photosynthesis; Fv /Fm
(dimensionless) = maximum quantum yield of photosystem II; ETR (µmol m –2 s –1) = electron transport rate; NPQ (relative units) = non-photochemical quenching of chlorophyll fluorescence; [Chl] (mmol m –2) = concentration of chlorophyll; [VAZ] (mmol m –2) = concentration of
violaxanthin, antheraxanthin and zeaxanthin. Treatments: C = control; MD = mild drought; and SD = severe drought.
R. alaternus
C
g
165.0
bc
RWC 87.2
abc
LMA 136.1
abcd
[N]
1.98
def
11.5
AN
bc
AN/g 74.9
abc
φ
0.063
ab
k
19.3
a
1.2
RD
cd
Amax 26.1
bc
ε
0.066
bcde
Γ
74.6
abc
4.9
RL
bcde
l
0.43
abcdef
Fv/Fm 0.794
abcd
ETR 96.1
def
NPQ 2.7
bcd
[Chl] 22.5
efg
[VAZ] 10.5
abc
R. ludovici-salvatoris Q. ilex
Q. humilis
P. lentiscus
P. therebinthus
MD
SD
C
MD
SD
C
MD
SD
C
MD
SD
C
MD
SD
C
MD
SD
59.6
def
77.2
bcde
155.4
cde
2.12
cde
5.2
fghi
87.4
abc
0.042
bcdef
37.4
ab
1.5
cd
19.4
cde
0.044
defg
98.3
abcd
4.3
cde
0.51
abcdef
0.741
ef
64.9
fgh
3.9
def
30.1
bcdef
7.6
cdef
38.5
f
81.4
de
162.1
de
1.75
efg
4.2
ghi
113.9
c
0.048
abcdef
38.8
ab
1.8
cd
17.1
cdef
0.043
defg
103.3
bcd
4.5
bcde
0.62
def
0.736
f
44.9
gh
3.8
def
37.0
b
9.0
abcde
222.0
ab
88.9
abc
111.5
a
1.84
ef
10.9
cde
49.2
a
0.060
abcd
73.2
c
4.2
a
32.1
ab
0.080
bcd
96.7
abcd
7.8
ab
0.33
a
0.799
abcd
106.1
def
2.7
bcd
26.1
cdefg
7.4
cdef
115.5
cdef
82.2
bcde
145.1
bcde
1.76
efg
9.3
cde
83.1
abc
0.048
abcdef
46.3
abc
2.1
bcd
26.0
bc
0.064
bcdef
93.1
abcd
6.0
abcd
0.38
ab
0.791
abcd
74.4
efg
3.2
bcde
33.9
bc
9.5
abc
37.9
f
73.2
de
174.0
ef
1.65
fg
3.3
i
85.1
abc
0.033
cdef
43.0
abc
1.4
cd
16.7
cdef
0.037
efg
163.9
e
5.9
abcd
0.59
bcdef
0.737
f
80.0
def
3.3
bcde
45.5
a
4.8
f
277.8
a
80.3
cde
198.3
fg
1.34
hi
15.5
a
56.9
ab
0.060
abc
23.1
ab
1.4
cd
32.3
ab
0.089
bc
69.0
ab
6.2
abcd
0.39
a
0.816
ab
164.8
ab
2.3
abc
21.6
fg
5.9
def
112.3
cdef
82.7
bcd
200.3
fg
1.27
i
7.4
defgh
66.3
ab
0.032
def
52.1
bc
1.5
cd
14.8
cdef
0.070
bcde
79.1
abc
5.4
bcde
0.34
abcd
0.807
abc
105.3
cde
2.9
bcd
31.2
bcde
5.8
ef
42.8
f
73.2
e
217.7
g
1.21
i
3.7
hi
87.5
abc
0.027
f
41.5
ab
1.1
cd
6.7
f
0.028
fg
117.5
d
3.3
de
0.53
abcdef
0.797
abcd
46.0
gh
3.8
def
26.9
cdefg
7.9
cdef
278.8
a
95.4
a
115.9
ab
2.59
a
16.0
a
57.9
ab
0.051
abcdef
37.7
ab
1.9
bcd
34.6
ab
0.099
abc
63.0
a
6.2
abcd
0.38
ab
0.824
a
184.2
a
2.0
ab
25.9
cdefg
9.2
abcd
134.0
cd
92.3
a
113.0
a
2.31
bc
8.8
cdef
66.1
ab
0.071
a
45.5
abc
3.3
ab
15.4
cdef
0.057
cdefg
89.9
abcd
5.1
bcde
0.36
abcdef
0.825
a
78.4
def
4.2
ef
27.3
cdefg
9.8
abc
47.2
ef
88.4
abc
116.4
ab
2.00
de
4.0
hi
83.9
abc
0.031
ef
28.8
ab
0.9
d
8.5
ef
0.059
cdef
93.1
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Effects of drought treatment and species on photosynthetic
parameters
Because Pearson’s correlation analyses indicated that φ, k and
RD were not correlated with other parameters, including RWC
and g, these parameters were not considered further. Several
parameters that were significantly correlated with g were also
significantly correlated with other parameters (P < 0.001).
Among these, ETR showed a highly significant negative cor-
relation with NPQ, whereas Amax, ε and Γ were all strongly interrelated. Moreover, Amax, ε and Γ were significantly
correlated with ETR.
A summary of the ANOVA of the effects of treatment, species and treatment × species interaction on selected photosynthetic parameters is shown in Table 3. Drought significantly
affected each parameter presented in Table 3, whereas the
interspecific variation was only significant for RL and Fv /Fm.
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Table 2. Two-way ANOVA of the effects of treatment, species and
treatment × species interaction on mid-morning stomatal conductance
(g), predawn leaf relative water content (RWC), leaf mass area
(LMA) and leaf nitrogen concentration on a dry mass basis ([N]).
Parameter
Treatment
P-value
Species
P-value
Treatment × species
P-value
g
RWC
LMA
[N]
< 0.001
0.104
0.077
< 0.001
0.044
0.059
< 0.001
< 0.001
0.024
< 0.001
< 0.001
< 0.001
The treatment × species interaction had a significant effect on
all parameters presented in Table 3, except RL, suggesting species-dependent differences in the RL response to drought. Figures 3 and 4 show parameters that were significantly affected
by treatment × species interaction.
The response of AN to drought followed that of g (Figures 3A–C), except in drought-treated plants of R. ludovicisalvatoris, which maintained an almost constant AN in control
plants and in plants subjected to mild drought (Figure 3A).
Among species in the well-watered treatment, R. ludovicisalvatoris had the lowest intrinsic water-use efficiency (AN /g)
(Figure 3D). In all species, AN /g increased with decreasing g
and AN (Figures 3D–F), reaching maximum values in plants in
the severe drought treatment. Among species in the mild and
severe drought treatments, the highest AN /g values were found
in R. alaternus and P. lentiscus, and the lowest values were
found in P. terebinthus. Stomatal limitation (l ), calculated
from AN –Ci curves, showed a similar pattern to that of AN /g
(Figure 3G–I).
Drought caused decreases in Amax (Figure 4A–C), ε (Figure 4D–F) and ETR (Figure 4G–I). The drought-induced declines in these parameters followed a similar pattern in all
species, although the relative decreases were slightly higher in
Figure 2. Relationship between predawn leaf relative water content
(RWC) and mid-morning stomatal conductance (g) for: 䉮, Rhamnus
ludovici-salvatoris; 䊊, R. alaternus; 䉭, Quercus ilex; 䉱, Q. humilis;
䊐, Pistacia lentiscus; and 䊏, P. terebinthus.
Table 3. Two-way ANOVA of the effects of treatment, species and
treatment × species interaction on the photosynthetic parameters
found to correlate with stomatal conductance. Abbreviations: AN
(µmol m –2 s –1) = net CO2 assimilation; A/g (µmol mol –1) = intrinsic
water-use efficiency; Amax (µmol CO2 m –2 s –1) = light- and CO2-saturated photosynthesis; RL (µmol m –2 s –1) = the sum of photorespiration and mitochondrial respiration in the light; l (dimensionless) =
stomatal limitation to photosynthesis; ETR (µmol m –2 s –1) = electron
transport rate; Fv /Fm (dimensionless) = maximum quantum yield of
Photosystem II.
Parameter
Treatment
P-value
Species
P-value
Treatment × species
P-value
AN
AN /g
Amax
RL
l
ETR (NPQ)
Fv /Fm
< 0.001
0.025
< 0.001
0.004
0.010
< 0.001
0.031
0.266
0.201
0.191
0.024
0.089
0.244
0.015
< 0.001
0.027
< 0.001
0.069
0.007
< 0.001
< 0.001
the Quercus and Pistacia species (60–80%) than in the Rhamnus species (40–50%).
Pigment composition and its relationship with photochemistry
Some interspecific and treatment-dependent differences were
observed in leaf pigment composition. Area-based total chlorophyll concentration differed markedly among species (Table 1), but variations between drought treatments were small.
For the two Rhamnus species, there was a progressive increase
in chlorophyll concentration paralleling the increase in soil
water depletion; however, this could simply be a consequence
of interannual differences. The total VAZ (sum of violaxanthin, antheraxanthin and zeaxanthin) pool as a proportion of
chlorophyll concentration was species-dependent, but was
hardly affected by the drought treatments (Table 1).
All of the species had a drought-induced sustained DPS at
predawn (Figure 5A), ranging from 0.12 to 0.23. Predawn
DPS was related to low Fv /Fm only in the three shrub species,
whereas the tree species maintained an Fv /Fm close to 0.8, irrespective of DPS (Figure 5A). A correlation between midmorning NPQ and DPS was observed when the six species
were considered together (Figure 5B); however, there was no
correlation between these parameters if only the Rhamnus species were considered. The two Rhamnus species had maximum DPS values even during irrigation. If only the four desiccation-avoiding species are considered, the correlation
improves (r 2 = 0.67, P < 0.01). Maximum DPS was similar
(0.8–0.9) for five of the study species, but was lower (0.65)
for R. ludovici-salvatoris, which was also the only species that
showed no increase in NPQ in response to drought, and high
ETR even during severe drought (Figure 4G).
Discussion
Relationship between g and RWC
The study species fell into two groups on the basis of their re-
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693
Figure 3. Drought effects on mean values of net CO2 assimilation (AN; A–C), intrinsic water-use efficiency (AN /g; D–F) and stomatal limitation
(l; G–I) in the two Rhamnus species (A, D, G), the two Quercus species (B, E, H) and the two Pistacia species (C, F, I). Values are means ± SE of
four replicates. Within a species and parameter, different letters indicate significant differences between treatments (P < 0.05).
sponse to soil water depletion; dessication-tolerant species
and dessication-avoiding species. Both Rhamnus species exhibited simultaneous decreases in g and RWC, which is typical of desiccation-tolerant species (Gucci et al. 1997, Martínez-Ferri et al. 2000). The Quercus and Pistacia species
achieved 50% stomatal closure before showing a reduction in
predawn RWC. This rapid stomatal response to soil drying
may enable these species to delay dehydration so, at least with
respect to this characteristic, they can be considered desiccation-avoiding species. Other studies have identified P. lentiscus (Tenhunen et al. 1987, Gucci et al. 1997), Q. humilis
(Damesin et al. 1998, Schwanz and Polle 1998, Nardini and
Pitt 1999) and Q. ilex (Sala and Tenhunen 1996, Damesin et al.
1998) as drought-avoiding species, although the latter species
has also been described as desiccation-tolerant (Sala and Tenhunen 1994). The desiccation-avoiding trait may impose a serious constraint on the winter deciduous species P. terebinthus
and Q. humilis, because it implies that they close their stomata
rapidly at the onset of drought, thus severely limiting carbon
assimilation during the summer. For the evergreen species,
P. lentiscus and Q. ilex, this trait may not constrain year-round
assimilation as much as it does in the two deciduous species
because the evergreen species maintain photosynthetic activity during winter (Damesin et al. 1998, Joffre et al. 1999).
These photosynthetic differences may explain why P. terebinthus is rare and limited to humid places (Castro-Díez et al.
1998), and why Q. humilis is absent in Mallorca and other arid
Mediterranean zones (Ne’eman and Goubitz 2000).
Desiccation tolerance in the Rhamnus species facilitates
maintenance of high assimilation rates during the onset of water deficit. However, the disadvantage is that the plants desiccate progressively during the summer. In the present study,
R. ludovici-salvatoris saplings lost 15% of leaf RWC in
5 days. During especially dry and long summers, survival of
adult trees as well as seedlings may be threatened.
Leaf photosynthetic capacity
The photosynthetic characteristics of Mediterranean evergreen trees and shrubs are reported to be similar (Ehleringer
and Mooney 1982). However, although we found that Amax
was similar in well-watered plants of all the study species, the
highest g, AN and ε were found in the tree species, and the
highest intrinsic water-use efficiency (AN /g) was found in the
shrub species. Our findings suggest that g and perhaps mesophyll conductance, but not photosynthetic capacity, were the
main determinants of interspecific differences in AN (cf. Epron
et al. 1995, Syversten et al. 1995).
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Figure 4. Drought effects on mean values of light- and CO2-saturated CO2 assimilation (Amax; A–C), apparent carboxylation efficiency (ε; D–F)
and electron transport rate (ETR; G–I) in the two Rhamnus species (A, D, G), the two Quercus species (B, E, H) and the two Pistacia species (C, F,
I). Values are means ± SE of four replicates. Within a species and parameter, different letters indicate significant differences between treatments
(P < 0.05).
Rhamnus ludovici-salvatoris was an exception among the
study species, with both low maximum photosynthetic rates
and intrinsic water-use efficiency under irrigation. Moreover,
it had the highest light respiration rates, indicating a disadvantageous carbon balance and low electron-use efficiency. These
photosynthetic characteristics imply that R. ludovici-salvatoris has relatively low resource-use efficiency, in addition to
low rates of Amax. Together these ecophysiological characteristics could account for the low competitiveness of this species,
even under favorable conditions, compared with the others
studied.
The adjustments in Amax and ε to drought were similar in all
the species, suggesting that these non-stomatal limitations to
photosynthesis do not determine interspecies differences in
acclimation to arid conditions. This is consistent with the progressive increases in AN /g and l as drought progressed. Only
P. lentiscus had a decrease in AN/g in response to severe
drought, but this species had the lowest g (37 mmol H2O m –2
s –1), which may have been below the inflexion point of the response of AN/g to g (Martin and Ruiz-Torres 1992, Flexas et al.
2002). High values of AN/g (up to 120) have been measured in
field-grown P. lentiscus at g values of 50 mmol H2O m –2 s –1 in
midsummer (Flexas et al. 2001).
Leaf photochemistry and xanthophyll cycle
The relationship between midday DPS and NPQ differed between the desiccation-avoiding and desiccation-tolerant species. In the four desiccation-avoiding species, there was a high
correlation between DPS and NPQ at mid-morning, as previously described for many species (Demmig et al. 1988, Johnson et al. 1993, García-Plazaola et al. 1997). However, this
correlation was not observed in the two desiccation-tolerant
Rhamnus species, which showed maximum DPS regardless of
their water status. Similar findings have been reported by
Munné-Bosch and Alegre (2000) for the Mediterranean species Lavandula stoechas L. However, the two Rhamnus species showed distinct de-epoxidation patterns. Among the
study species, R. alaternus had the highest DPS values, and increased NPQ in response to drought. We hypothesize that, in
this species, as in L. stoechas (Munné-Bosch and Alegre
2000), a high DPS, even in well-watered plants, represents a
strategy for coping with rapidly induced (days to weeks)
drought events typical of Mediterranean climates. In contrast,
R. ludovici-salvatoris had the lowest de-epoxidation capacity
among the study species, which was accompanied by low
NPQ and, consequently, a high electron transport rate even
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DROUGHT AND PHOTOSYNTHESIS IN MEDITERRANEAN SPECIES
695
Conclusions
We analyzed several photosynthetic characteristics and their
response to drought in Rhamnus ludovici-salvatoris, an endemic shrub of the Balearic Islands that is declining in distribution, and compared the values with those of several widely
distributed species. We found that R. ludovici-salvatoris displayed several traits that limit plant biomass production under
semi-arid conditions, including high ratios of respiration and
photorespiration to photosynthesis and a low intrinsic water-use efficiency that was not linked to a high photosynthetic
rate. Stomatal closure at the onset of water deficit was also delayed in this species. Moreover, among the six study species,
R. ludovici-salvatoris had the lowest de-epoxidation state of
the xanthophyll cycle and the lowest thermal dissipation.
These unfavorable photosynthetic traits may result in lower
carbon gains under favorable conditions, a lower capacity to
adjust photosynthesis under drought conditions, and lower
photoprotection ability even during drought, compared with
the other study species. It is well known that anthropogenic
factors account for most landscape degradation in the Balearic
Islands (Morey and Martínez 2000). Thus, the photosynthetic
traits displayed by R. ludovici-salvatoris may contribute to its
low rates of establishment and recovery after degradation. The
deciduous species studied did not display the same photosynthetic traits as R. ludovici-salvatoris, therefore, their low distribution in the Balearic Islands is probably related to the absence of carbon gain during winter. In addition, their droughtavoiding characteristics will strongly limit their ability to accumulate carbon during summer in arid locations.
Figure 5. (A) Relationship between predawn Fv /Fm and predawn deepoxidation state of the xanthophyll cycle (DPS) for the six species
studied. Separate correlations are shown for microphyll trees and
nanophyll shrubs. (B) Relationship between mid-morning NPQ and
mid-morning DPS for the six species studied. Separate correlations
are shown for drought-avoiding species and drought-tolerant species.
Each value is the mean of six measurements. Symbols: 䉮, Rhamnus
ludovici-salvatoris; 䊊, R. alaternus; 䉭, Quercus ilex; 䉱, Q. humilis;
䊐, Pistacia lentiscus; and 䊏, P. terebinthus.
Acknowledgments
This work is part of Projects CICYT PB97-1174 and PB97-1176, supported by the Spanish Ministry of Education and Science. J.F. was
supported by the UIB with a Beca d’Investigació. J.G. was supported
by the Project FEDER IFD97-0551. We are indebted to Dr. E. Descals and to Dr. M. Ribas-Carbó for grammar corrections.
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