Download Drought and warming induced changes in P and K concentration

Plant Soil (2008) 306:261–271
DOI 10.1007/s11104-008-9583-7
REGULAR ARTICLE
Drought and warming induced changes in P and K
concentration and accumulation in plant biomass and soil
in a Mediterranean shrubland
J. Sardans & J. Peñuelas & P. Prieto & M. Estiarte
Received: 28 September 2007 / Accepted: 26 February 2008 / Published online: 13 March 2008
# Springer Science + Business Media B.V. 2008
Abstract A field experiment involving drought and
warming manipulation was conducted over a 6-year
period in a Mediterranean shrubland to simulate the
climate conditions projected by IPCC models for the
coming decades (20% decreased soil moisture and 1°C
warming). We investigated P and K concentration and
accumulation in the leaves and stems of the dominant
species, and in soil. Drought decreased P concentration
in Globularia alypum leaves (21%) and in Erica
multiflora stems (30%) and decreased K concentration
in the leaves of both species (20% and 29%,
respectively). The general decrease of P and K
concentration in drought plots was due to the reduction
of soil water content, soil and root phosphatase activity
and photosynthetic capacity that decreased plant uptake
capacity. Warming increased P concentration in Erica
multiflora leaves (42%), but decreased it in the stems
and leaf litter of Erica multiflora and the leaf litter
(33%) of Globularia alypum, thereby demonstrating
that warming improved the P retranslocation and
allocation from stem to leaves. These results correlate
Responsible Editor: Hans Lambers.
J. Sardans (*) : J. Peñuelas : P. Prieto : M. Estiarte
Ecophysiology and Global Change Unit
CSIC-CEAB-CREAF, CREAF (Center for Ecological
research and Forestry Applications),
Universitat Autònoma de Barcelona,
08193 Bellaterra, Spain
e-mail: [email protected]
with the increase in photosynthetic capacity and
growth of these two dominant shrub species in
warming plots. Drought and warming had no significant effects on biomass P accumulation in the period
1999–2005, but drought increased K accumulation in
aboveground biomass (10 kg ha−1) in Globularia
alypum due to the increase in K concentration in
stems. The stoichiometric changes produced by the
different responses of the nutrients led to changes in
the P/K concentration ratio in Erica multiflora leaves,
stems and litter, and in Globularia alypum stems and
litter. This may have implications for the nutritional
value of these plant species and plant–herbivore
relationships. The effects of climate change on P and
K concentrations and contents in Mediterranean ecosystems will differ depending on whether the main
component of change is drought or warming.
Keywords Climate change . Drought .
Erica multiflora . Fertility . Globularia alypum .
Global change . Biomass K concentration .
Nutrient availability . Nutrient content .
Biomass P concentration . Sclerophylly . Warming .
Water stress
Introduction
Shrublands represent 17% of the surface in Catalonia,
which is almost half of the surface occupied by forest.
Shrublands represent, thus, a large percent of natural
262
vegetation and their response to climate change may
affect nutrient retention capacity at a regional scale.
Water is the most limiting factor in these Mediterranean
shrublands. Current climate and ecophysiological models such as Gotilwa (IPCC 2007; Sabaté et al. 2002;
Peñuelas et al. 2005) predict increased warming and
drought for the future in Mediterranean ecosystems.
Over the last century, temperatures in the Mediterranean Basin have already shown trends towards overall
warming (Peñuelas et al. 2002, 2005; Peñuelas and
Boada 2003). Precipitation has already begun to
exhibit either a long-term downward trend, mainly in
the dry season (Esteban-Parra et al. 1998), or no
significant change (Piñol et al. 1998; Peñuelas et al.
2002, 2005), although in all cases a rise in the
evapotranspiration potential has occurred, leading to
increased aridity (Piñol et al. 1998; Peñuelas et al.
2005).
Although human activities have increased P, K and
other nutrient inputs to terrestrial ecosystems in the
Mediterranean Basin (Peñuelas and Filella 2001),
nutrients are still limiting factors in Mediterranean
ecosystems (Hanley and Fenner 2001; Sardans and
Peñuelas 2004; Sardans et al. 2004, 2005a, b). Among
the different nutrients, P and K tissue concentrations
play a highly significant role in plant biology (Paoli et
al. 2005) and have been reported to be inversely
correlated to water availability (Díaz and Roldan
2000). Furthermore, Fernandez et al. (2006) have
observed that in the Mediterranean pine Pinus pinaster
growing in natural ecosystems in the centre of the
Iberian Peninsula, a decrease in the P supply led to
increased stomatal conductance and hence lower water
use efficiency (WUE). K is especially important in dry
environments due to its role in controlling leaf water
losses. In Mediterranean phanaerophytes, K use and
remobilization is related to osmotic requirements
(Milla et al. 2005). During the early stages of tree
establishment and in the course of a density manipulation field experiment, Gakis et al. (2004) observed a
significant positive correlation between tree growth
and K concentration in leaves in a young Mediterranean silvopastoral system in northern Greece. Similarly, Hanley and Fenner (1997) observed that K
availability limited biomass growth in some shrub
species in Californian Mediterranean shrublands. Several experiments have observed the positive effects of
K on plant drought resistance in natural ecosystems
(Egilla et al. 2005) and in crops (Stone and Moreira
Plant Soil (2008) 306:261–271
1996). In spite of such information, the global effects
of drought and warming on the P and K-cycle in
Mediterranean ecosystems and on the P and K stocks
in the different ecosystem compartments have not been
studied.
In order to understand the effect of the drought and
warming projected by IPCC models, it is essential to
investigate their effects on P and K availability in the
mid- and long term. To test warming and drought
effects on Mediterranean shrublands, an experiment
of warming and drought simulations has been
conducted in the Garraf Mountains (Catalonia,
north-east Spain) since 1999 (Peñuelas et al. 2007).
In this long-term field experiment, warming produced
a slight increase in growth of Erica multiflora and an
increase in photosynthetic capacity in the other
dominant shrub species, Globularia alypum (Llorens
et al. 2004a) and increased soil phosphatase activity
(Sardans et al. 2006a). After the first seven experimental years, warming had increased the stem growth
of Erica multiflora (30%; Peñuelas et al. 2007).
Drought decreased shoot water potential and stomatal conductance (Llorens et al. 2003), root-surface
phosphatase activity (Sardans et al. 2007) and net
photosynthetic rates of one of the two dominant shrub
species Erica multiflora (Llorens et al. 2004a), and
reduced the growth of both dominant shrub species,
Erica multiflora and Globularia alypum (24% and
39%, respectively) (Peñuelas et al. 2007). Moreover,
sclerophylly usually increases when the environment
evolves towards drier conditions (Sardans et al. 2006b)
leading to an accumulation of recalcitrant organic
matter in soil that may slow down organic matter
decomposition (Pastor et al. 1984; Coûteaux et al.
2002). Drought may reduce microbial enzyme activity,
although the forecasted global warming (IPCC 2007;
Sabaté et al. 2002; Peñuelas et al. 2005) may have the
opposite effect (Sardans et al. 2006a).
According to these previous results, a rise in plant
P and K uptake was expected under warming because
of the increase in soil enzyme activity (Sardans et al.
2006a), the increase in plant growth and photosynthetic capacity and the increase in retranslocation due
to the heightened resource demands from the photosynthetic and growing tissues. On the other hand,
the decrease in soil moisture in drought plots limits
the soil nutrient diffusion capacity and decreases the
activities of some soil enzymes (Sardans et al. 2006a)
and of plant root enzymes (Sardans et al. 2007). This,
Plant Soil (2008) 306:261–271
together with the reduced growth can limit the plant’s
capture capacity, decrease the aboveground P and K
contents and increase the soil contents and the
vulnerability to P and K losses from the ecosystem.
The decrease in growth can contribute to a concentration effect and the changes in leaf photosynthetic
capacity and in transpiration fluxes can change the
leaf–stem allocation. All these previous results also
indicate that drought and warming could affect the P
and K contents in soil and in plants differently
depending on the species-specific responses to
drought and warming.
Based on the previous data, we hypothesized that
(a) drought would increase total soil P and K
concentrations and would reduce P and K accumulation in stand biomass by reducing soil moisture, soil
diffusion capacity, plant-available P and K forms and
plant growth, and (b) warming would increase soil
nutrient availability, P and K accumulation and P
and K allocation to different plant organs, as a consequence of the observed increase in soil microbe
activity and by the enhancement of physiological
plant activity and growth. To test these hypotheses we
analyzed P and K in leaves and stems of the two
dominant species and in soil after a 6-year field
experiment in the Garraf Mediterranean shrubland in
which the drought (average 20% decreased soil
moisture) and warming (+1°C) conditions projected
for the coming decades by GCM and ecophysiological models (IPCC 2007; Sabaté et al. 2002; Peñuelas
et al. 2005) were simulated.
Materials and methods
Study site
The study was carried out in a natural Mediterranean
calcareous shrubland on a south-facing slope in the
Garraf mountains in central Catalonia (NE Spain; 41°
18′N, 1°49′E). The site is located on formerly
cultivated terraces – abandoned approximately a
century ago – with a Petrocalcic calcixerept soil (Soil
Survey Staff 1998) lying on bedrock of sedimentary
limestone, with a pH of 7.7 in water extracts. During
the study period (1999–2005) the average annual
temperature was 15.1°C (7.4°C in January and 22.5°C
in July) and the average annual rainfall 580 mm. The
summer drought is pronounced and usually lasts for
263
three months. The zone vegetation type was described
in Sardans et al. (2006a). Erica multiflora represents
ca. 20% and Globularia alypum ca. 33% of the total
surface area.
Experimental design and biomass accumulation
Treatments were established in nine plots, three plots
for warming, three plots for drought and three plots
for control. Plots were 4×5 m but 0.5 m were
measured as edge, so the effective plot area was
12 m2 (Peñuelas et al. 2004). The plots were
distributed in three blocks (each one with one control,
drought and warming). This was done to study
possible differences between the distant plots in spite
of the reduced area where the nine plots were
established (approximate 0.5 ha) and the homogeneity
of the plant community studied. The warming and
drought treatments and climate variable measurements are described in previous reports (Peñuelas et
al. 2004; Sardans et al. 2006a). Briefly, the warming
treatment was performed as nighttime warming by
reflective curtains covering the vegetation at night
(Beier et al. 2004). The covering of the ecosystem
with reflective curtains reduces the loss of IR
radiation. The warming plots are covered by a light
scaffolding that supports the reflective aluminum
curtains. The coverage of the study plots is activated
automatically according to preset light (less than
200 lx), rain, and wind (less than 10 m s−1) conditions
(Beier et al. 2004). To avoid influencing of the
hydrological cycle, the covers, triggered by rain
sensors are automatically removed during rain events.
The warming treatment has been applied since spring
1999 and is lasting until now. Drought treatment was
performed for the growing periods of spring and
autumn by covering the vegetation with waterproof,
transparent covers. The curtain material is a transparent plastic and the moving of the curtains is governed
only by rain and wind. During the drought period, the
rain sensors activate the curtain to cover the plots
whenever it rains and to remove the curtains when the
rain stops. The curtains are removed automatically if
the wind speed exceeds 10 m s−1. For the part of the
year without drought treatment, the drought plots
were run parallel to the control plots.
In 1999 and 2005, biomass per plot was estimated
by means of the pin point method as described by
Peñuelas et al. (2007).
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Sampling process
Samples for plant chemistry were obtained at the
beginning of the experiment in January 1999, before
treatments started, and six years later in January 2005.
Each sampling involved five individual plants from
each plot of the two dominant shrub species, Erica
multiflora and Globularia alypum. Five branches
were sampled from each plant. Since the leaf
population of Erica multiflora consisted of currentyear leaves and one-year-old leaves, for this species
we used two different leaf cohorts (current-year and
one-year-old). In Globularia alypum, since only
current-year leaves were present during the sampling
campaign only one cohort of leaves was considered.
Two fractions of aboveground biomass were considered in Globularia alypum (stem and current-year
leaves) and three (stem, current-year leaves, and 1year old leaves) in Erica multiflora. For root biomass
three sample cores (30 cm deep) were obtained from
each plot. Due to the difficulty of distinguishing
between the roots of different species we sampled
near Globularia alypum and only collected roots of
this species. In each core we selected the roots of φ<
1 mm and the roots of φ>1 mm that were analyzed
separately.
The litterfall of 4–8 plants of Erica multiflora and
9–12 plants of Globularia alypum per plot was
monitored during 1999 and 2004. Plant litterfall was
collected bimonthly by means of open collectors
located under each selected plant. Samples were dried
to constant weight and afterwards separated and
weighed.
The P and K content of each biomass fraction and
species for each plot was calculated by multiplying
their corresponding concentration in the biomass
fraction by the corresponding biomass per plot. In
the case of Erica multiflora, we only used the
concentration in the current-year leaves to calculate
the leaf nutrient content since in this species this leaf
cohort represented most of the leaf biomass when
sampling.
For the soil analyses, three sample cores (30 cm
deep) from each plot were taken in January 2005 to
analyze P and K concentration in soil. For the rock
analyses, 18 rock samples were collected (two near
each plot where the bedrock reached the surface) to
analyze P and K concentrations in bedrock. Before
starting the experiment in January 1999 we conducted
Plant Soil (2008) 306:261–271
analyses of the soil concentration of several elements
in the area where the plots were thereafter established
(control, drought and warming plots) and no differences were detected in the P and K contents among
soil samples.
All the samples were taken to a laboratory and
stored at 4°C until analysis. In order to analyze only P
and K in the foliar tissue, leaves were washed with
distilled water Porter (1986). After all samples had
been washed, they were dried in an oven at 60°C until
constant weight was reached and then were ground in
a Cyclotec 1093 (Foss Tecator, Höganäs, Sweden;
plant biomass) or in a Fritsch Pulverisette (Rudolstadt,
Germany; soils and bedrock).
Chemical analyses
The concentrations of P and K in all plant samples
and soil samples were measured using ICP-OES
(optic emission spectroscopy with inductively coupled
plasma) in a JOBIN IBON JY 38 (Longjumeau,
HORIBA Jobin Ibon S.A.S., France). Before the
plant sample ICP-OES analyses, an acid digestion of
the plant samples was carried out with an acid mixture of HNO3 (60%) and HClO4 (60%; 2:1) in a
microwave oven (Samsung, TDS, Seoul, South
Korea). Two milliliters of the mixed acid solution
were added to 100 mg of each dried plant sample.
The digested solutions were made up to 10 ml final
volume. During the acid digestion process, two
blank solutions (2 ml of acid mixture without any
sample biomass) were also analyzed. In order to
assess the accuracy of plant sample digestion and
analytical procedures, we used standard certified
biomass (DC73351; poplar leaf, purchased from the
China National Analysis Center for Iron and Steel).
For the determination of total P and K concentrations
in soil and bedrock samples, digestion was carried
out with 0.25 g of ground sample in 9 ml of HNO3
(65%) and 4 ml HF (40%) in a microwave oven at
120°C for 8 h (Bargagli et al. 1995). The digested
solutions were made up to 50 ml final volume,
filtered with a Millex 0.45 μm filter, and then stored
at 4°C until analysis. The precision of the soil and
bedrock analyses, as verified by parallel analyses of a
standard certified rock GSR-6 (Carbonate rock,
purchased from the Institute of Geographical and
Geochemical Prospecting of China), was better than
5% for both P and K.
Plant Soil (2008) 306:261–271
265
performed a Bonferroni/Dunn post-hoc ANOVA test
to analyze how each treatment affected P and K
concentrations and contents in soil, litter, and biomass. For all analyses the Statview 5.1 package
(Abacus Concepts, Inc., Berkeley) was used.
Soil P and K concentrations
The plant’s available-P was determined by Olsen’s
method (Watanabe and Olsen 1965). This method
measures inorganic P extracted in 0.5 M NaHCO3 at
pH 8.5 (Olsen Pi). Total P in the extract (Olsen Pt)
was determined in an aliquot of extract after adding
an equal volume of 5 N H2SO4 containing 167 g
KS2O8 l−1 and digesting at 150°C. Organic-P in the
extract (Olsen Po) was calculated by difference
between Olsen Pt and Olsen Pi.
We analyzed K concentrations in soil extract in
each soil sample by following van Elteren and Budic
(2004). Briefly, extracts were obtained by shaking 2 g
of soil with 10 ml of solvent (0.01 M NaN03). The
soil was mixed with the 0.01 M NaNO3 solvent in 50ml plastic centrifuge tubes. Two suspensions were
prepared for each sample. The soil mixtures were
equilibrated by shaking on a reciprocal shaker at 100
strokes per minute for 5 h, a technique based on batch
extraction studies by Gupta and Mackay (1966). After
equilibrium, soil solids were separated from the
solution by centrifugation and filtration through a
0.45 μm pore-size membrane filter. The concentrations of K in the filtered extracts were determined as
described in the biomass, soil, and bedrock digests.
Results
Soil
During the six years the study lasted (1999–2005), the
drought treatment led to a mean reduction in soil
moisture of 20.6% with respect to the control
treatment. A significant decrease in soil moisture
occurred in drought plots in spring and autumn rainy
seasons with the drought treatment running (Fig. 1).
During the period 2001–2004 the average T increase
in the warming treatment was 0.95°C at a depth of
−5 cm and 0.75°C in the air (20 cm), but the warming
treatment had no effect on soil moisture during the
6 years of study. Winter was the season with the
greatest effects of warming (Fig. 1). In winter soil
temperatures were 1.20±0.09°C higher than in control soil, whereas in summer they were 0.77±0.08°C
higher (Fig. 1, for years previous to 2002 see Llorens
et al. 2004b).
Drought treatment tended to increase the total soil P
content and non-labile soil P fraction (non-Olsen-Ptotal;
Table 1). Warming tended to reduce total soil P and
non-Olsen-Ptotal with respect to control plots. No
Statistical analyses
The effects of the treatments on each variable studied
were investigated by means of ANOVA analyses. We
25
*
*
*
*
2002
2003
Year
*
*
June
April
* * **
February
*
Decem.
October
June
August
Control
Drought
Warming
**
April
*
*
*
February
October
August
*
*
*
*
*
Decem.
*
June
* *
* *
*
*
* *
April
30
25
20
15
10
5
*
2004
**
Decem.
10
*
*
October
*
15
August
20
February
Soil moisture
(%, v/v)
30
Soil T (°C) at 5 cm
soil depth
Fig. 1 Monthly mean soil
water content (% v/v±SE;
0–15 cm of soil depth) and
temperatures (°C±SE; at
5 cm of soil depth) of
control, drought and warming plots throughout 2001–
2004 (for soil water content)
and throughout 2002–2004
(for temperatures). Significant differences (P<0.05,
t-test) of soil water content
between drought plots and
control plots and significant
differences of soil temperature between warming plots
and control plots are indicated by asterisks
266
Plant Soil (2008) 306:261–271
Table 1 Concentrations (mean±SE) of P (μg g−1) and K (mg g−1) in soils in January 2005, after 6 year experimentation
Element Factor
P
K
Total
P soil
Total K
P-NonNaHCO3- soil*
extractable
Pi(NaHCO3)- Po(NaHCO3)- (Pi/Po)extractable
extractable
NaHCO3
Control
131±18ab 1.51±0.6
Drought 161±29a 1.30±0.4
Warming 83±20b 2.90±0.9
Control
Drought
Warming
75±14
74±6
63±6
K-(NaNO3)extractable*
K-non
(HaNO3)extractable*
0.030±0.011 54.5±13ab
0.016±0.005 91.7±19a
0.037±0.011 20.2±14b
6.28±0.19 0.049±0.005 6.24±0.19
6.43±0.31 0.044±0.007 6.39±0.30
5.66±0.32 0.040±0.003 5.62±0.29
Different letters indicate significant statistical differences between treatments (p<0.05, post-hoc Bonferroni–Dunn test, ANOVA).
They are highlighted in bold type.
Biomass
The block factor had no significant effects in any of
the variables studied (P and K contents and concentrations in plants and soils).
In Erica multiflora and in the period 1999–2005,
neither warming nor drought had a statistically
significant effect on total accumulated biomass (290±
197, 143±47 and 381±236 kg ha−1 in leaves and
668±358, 292±87 and 1,066±563 kg ha−1 in stems,
in control, drought and warming plots, respectively).
In Globularia alypum and in the period 1999–2005,
neither warming nor drought had a statistically
significant effect on total accumulated biomass (382±
249, 263±28, 61±164 kg ha−1 in leaves). There was a
marginally significant (P=0.098) increase of stem
biomass accumulation in the drought plots (643±153,
1712±490, 1,023±44 kg ha−1 in control, drought and
warming plots, respectively).
Both Erica multiflora and Globularia alypum
presented significant differences in P and K concentrations in the different plots at the beginning of the
experiment (data not shown).
In Erica multiflora drought decreased P concentration in stems (0.073 mg g−1, 31±3%, P=0.04) and
decreased K concentration in both current-year leaves
(1.19 mg g−1, 27±2%, P=0.01), and 1-year-old leaves
(1.25 mg g−1, 30±3%, P=0.004; Figs. 2 and 3). The
warming treatment increased P concentration in
current-year leaves (0.05 mg g−1, 42±11%, P=0.03)
and decreased P concentration in leaf litter (0.08 mg
g−1, 64±11%, P=0.005; Fig. 2).
In Globularia alypum drought decreased P (0.087 mg
g−1, 21±6%, P=0.04) and K (1.38 mg g−1, 21±7%,
P=0.03) concentrations in leaves (Figs. 2 and 3) and
increased K concentration in stems (1.83 mg g−1, 35±
6%, P=0.01; Fig. 3). Warming decreased P concentration in leaf litter (0.11 mg g−1, 34±5%, P=0.03;
Erica multiflora
0.5
Control
Drought
Warming
0.4
0.3
P concentration (mg g-1)
effects of drought or warming were observed on total
soil K, extractable K, or on non-extractable K (Table 1).
0.2
a
b ab
a
b ab
a
0.1
a
b
0
Current-year One-year-old
leaves
leaves
Litter
Stems
Stems
Roots
Globularia alypum
0.8
0.6
a
0.4
a
b
a
ab
b
0.2
0
Leaves
Litter
Biomass fraction
Fig. 2 P concentrations (mg g−1) in plant organs under the
different treatments in January 2005 in Erica multiflora and
Globularia alypum
Plant Soil (2008) 306:261–271
Erica multiflora
8
Control
Drought
Warming
a
a
ab
b
6
4
K concentration (mg g-1)
267
b
ab
2
0
Current-year One-year-old
leaves
leaves
6
Stems
Globularia alypum
10
8
Litter
a
a
b
ab
ab
P and K concentrations and contents
b
4
2
0
Leaves
published data on P and K concentrations in Erica
multiflora (Sardans et al. 2006c). The P concentrations in the present study (0.14±0.02 mg g−1 in
current-year leaves and 0.24±0.04 mg g−1 in stems)
are lower than those found in other shrublands in
Catalonia (0.380±0.010 and 0.51±0.02 mg g−1 in
current leaves and stems, respectively; Sardans et al.
2006c). These low biomass concentrations, together
with the low total soil P and bedrock P (20 μg g−1)
concentrations, indicate that P plays a limiting role in
this Mediterranean ecosystem, as has also been
observed in nearby communities of similar characteristics (Sardans et al. 2004).
Litter
Stems
Roots
Biomass fractions
Fig. 3 K concentrations (mg g−1) in plant organs under the
different treatments in January 2005 in Erica multiflora and
Globularia alypum
Fig. 2). Neither drought nor warming had any effects
on P and K concentrations in the roots of Globularia
alypum (Figs. 2 and 3).
Drought decreased the stem biomass accumulation
of K in Erica multiflora, and tended to decreased K
accumulation in leaves and P accumulation in leaves
and stems in this species, although the changes were
not significant (Fig. 4). In Erica multiflora warming
had no effects on P and K accumulation in aboveground biomass (Fig. 4).
In Globularia alypum drought did not affect P
accumulation in leaf and stem biomass (Fig. 4), but
increased K accumulation in stems (11.2 kg ha−1) and
in total aboveground biomass (10.3 kg ha−1; Fig. 4).
Warming had no effects on P and K accumulation in
aboveground biomass in this species (Fig. 4).
Discussion
Information on P and K concentrations in the two
species studied is scarce. To date there is only some
Drought decreased P and K plant biomass concentrations, except in the case of K concentration in
Globularia alypum stems. The reduction in soil
moisture and as a consequence the reduction in soil
and root phosphatases observed in drought plots during
some seasons (Sardans et al. 2006a, 2007) have
diminished the P soil mineralization, decreasing the
available P and increasing the concentration of non
available-P in soil.. These consequences of drought,
the reduction of soil phosphatase activity and P
mineralization, have also been observed in a Mediterranean forest located at 60 km from this experimental
site by Sardans and Peñuelas (2004, 2005). All these
data demonstrate that a moderate soil moisture decrease reduces soil enzyme activity by a direct soil
moisture effect in Mediterranean ecosystems (Sardans
et al. 2006b). However, drought reduced the capacity
to capture P not only because of the decrease of P
availability in soil, but also because of the decrease in
P uptake capacity due to the tendency to decrease
photosynthetic capacity (Llorens et al. 2004a). Plant
available-P is scarce in this community because of the
large presence of calcium carbonates and the high soil
pH. Therefore drought’s effect of reducing plant
available-P may be critical.
The consequences of drought were greater and
more general for K than for P, probably due to the fact
that K is more mobile in soil, its absorption is more
dependent on water transpiration and it is related to
plant osmotic control. The decrease in soil moisture in
drought plots implied a decrease in soil diffusion
capacity, diminishing the possibilities of plant K
capture. Several studies have also shown that drought
268
Plant Soil (2008) 306:261–271
Globularia alypum
Erica multiflora
0.5
0.4
0.6
Control
Drought
Warming
0.4
10
8
a
a
6
4
b
2
0
P
0.2
21
a
15
K
0.1
Absolute increment (kg ha-1)
P
0.2
K
Absolute increment (kg ha-1)
0.3
10
5
b
a
b
ab b
0
Leaves
Stems
Biomass fraction
Leaves
Stems
Biomass fraction
Fig. 4 P and K absolute (g ha−1) accumulation under the
different treatments during the period January 1999–January
2005 in Erica multiflora and Globularia alypum. Different
letters indicate significant statistical differences between different treatments (P < 0.05, post-hoc Bonferroni–Dunn test,
ANOVA)
reduces soil K release capacity (Kaya et al. 2005), and
thus it may decrease K availability in soils. Drought
tended to decrease P and K accumulation in the
aboveground biomass of Erica multiflora whereas on
the contrary, it increased K accumulation in the
aboveground biomass of Globularia alypum. The
greater accumulation in stem mass was linked mainly
to the greater K concentration and to a lesser extent to
a marginal increase in stem mass as a result of
drought. Drought induced lower transpiration rates
and stomatal conductance (Llorens et al. 2003). A
good correlation between K absorption capacity and
transpiration rates has been reported in other experiments (Marschner 1995). Leaves, on the other hand,
did show a decrease in K concentration despite the
trend towards less leaf mass accumulation. Thus,
there seems to be a greater K allocation to stems
under drought conditions in Globularia alypum, this
being the species less affected by drought. K
accumulation in stems might be an adaptation
mechanism to reduce water stress by raising leaf
water potentials and plant water retention capacity,
leading to a greater capacity for photosynthesis
(Sangakkara et al. 2000). These authors observed that
an increase in K availability, and the consequent
increase in stem K concentration, has a beneficial
effect in overcoming soil moisture stress. The
possible involvement of accumulation of K in stems
in an avoidance mechanism warrants further research.
Although in our previous study (Peñuelas et al.
2004) we found that warming decreased leaf P
concentration in Globularia alypum by 11% in 2001
(2 years after treatments started), in 2005, 6 years
after starting the warming treatment application, we
found that warming had no effect on foliar P
concentration in Globularia alypum but increased
current-year leaf P concentration in Erica multiflora
(42%). Changes in concentration depend on the
balance between nutrient and biomass change. Warming probably affected growth capacity more quickly
than it affected the mechanisms of P capture. Thus,
the effects on plant metabolic capacity were already
observable in the first years after the treatment
application, while the effects of warming increasing
P absorption (for example, changes in soil properties,
soil microbe activity, root growth, and/or root
architecture) were likely to have taken place at a
slower rate.
Plant Soil (2008) 306:261–271
Although warming increased leaf P concentration in
Erica multiflora, P decreased in stems and leaf litter. In
Globularia alypum warming also decreased P concentration in leaf litter thereby demonstrating that warming
enhanced the leaf P retranslocation and allocation from
stems to leaves. Erica multiflora showed a greater P
remobilization capacity in response to warming than
Globularia alypum, which was in accordance with the
greater growth response of Erica multiflora than
Globularia alypum in warming plots (Peñuelas et al.
2007). These results are directly correlated with the
increases in photosynthetic capacity of the two
dominant shrubs of this community in the warming
plots, especially in Erica multiflora (Llorens et al.
2003). Warming increased the potential photochemical
efficiency of PS II (Fv/Fm) in Erica multiflora and
Globularia alypum at predawn and midday (Llorens et
al. 2003) and the photosynthetic capacity in Globularia
alypum (Llorens et al. 2004a). Warming increased stem
growth, mainly in Erica multiflora (Peñuelas et al.
2007), an effect also related to the decrease in stem P
concentration observed in Erica multiflora. This effect
may have enhanced the retranslocation of water and
nutrients towards the leaves, especially in the case of P,
that is scarce in this community and is fundamental for
plant production capacity. On the other hand, in this
experiment, warming did not affect significantly the
plant transpiration rates (Llorens et al. 2003), and
therefore did not reduce significantly soil moisture nor
the water mass flux of K and P from soil to plants.
Thus, in warming plots the observed lower P content in
leaf litter in both Erica multiflora and Globularia
alypum and also the increased soil phosphatase enzyme
activity (Sardans et al. 2006a) explain the observed
tendency to decrease soil non-soluble-P (non-NaHCO3
extractable). On the other hand, under the warming
treatment, the increase in soil enzyme activity has not
been accompanied by an increase in plant available-P
in soil, nor by a significant increase in P accumulation
in the aboveground biomass of the two dominant shrub
species of the community. Increases in microbial
activity could explain this result since microbes are in
general better competitors for P than plants (Kellogg
and Bridgham 2001).
Possible implications for ecosystem processes
These changes in plant and soil P and K contents may
have several implications in diverse ecosystem process-
269
es. If more intense drought periods are accompanied by
more severe torrential rainfalls, as is predicted to occur
in the coming years (IPCC 2007; Peñuelas et al. 2005),
the tendency to increase P soil stocks under drought
makes P ecosystem losses from soil to continental
waters more likely. In fact, drought has been found to
increase P losses to continental waters in the terrestrial
temperate ecosystems of England (Bouraoui et al.
2004). Thus, the drought and the reduction in P stocks
in the ecosystems may have a synergic negative impact
on the future plant production capacity of Mediterranean ecosystems. The warming treatment increased P
soil mineralization and plant photosynthetic efficiency
(Llorens et al. 2004a) and tended to diminish total P in
soil. If there is warming without significant changes in
water availability, there will be increases in nutrient
mineralization and in nutrient remobilization that could
lead to an increase in the ecosystem’s capacity to
improve photosynthetic output and probably WUE in
the long term.
As a consequence of the different drought and
warming effects on P and K, the P/K concentration
ratio has decreased in the stems and leaf-litter of
Globularia alypum and Erica multiflora in warming
plots, whereas the P/K concentration ratio has
increased in the leaves of Erica multiflora in drought
and in warming plots. These different interspecific
responses to drought and warming of the stoichiometry between P and K in plant tissues may have
implications for their nutritional value and may affect
plant-herbivore relationships (Ngai and Jefferies
2004). Another additional implication that warrants
further study is that these fast changes in nutrient
ratios can favor species with a more flexible body
elemental composition. This could constrain the
ecosystem resistance to drought in this Mediterranean
ecosystem because the species with a flexible body
elemental composition generally have a low physiological efficiency in the use of environmental sources
(Jaenike and Markow 2003). Thus, the effects of
drought and warming on P and K stoichiometry may
influence plant competivity, trophic chains, and
finally, community structure and species composition.
Acknowledgements This research was supported by the
Spanish Government projects CGL2004-01402/BOS and
CGL2006-04025/BOS, the Catalan Government grant SGR
2005-00312, the European projects ALARM (Contract 506675)
and FP6 NEU NITROEUROPE (GOCE017841), and a Fundación BBVA 2004 grant.
270
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