Plant and Soil 267: 367–377, 2004.
© 2004 Kluwer Academic Publishers. Printed in the Netherlands.
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Increasing drought decreases phosphorus availability in an evergreen
Mediterranean forest
Jordi Sardans1,2 & Josep Peñuelas1
1 Unitat d’Ecofisiologia CSIC-CEAB-CREAF, CREAF (Center for Ecological Research and Forestry Applications),
Edifici C, Universitat Autònoma de Barcelona. Bellaterra 08193 (Barcelona), Spain. 2 Corresponding author∗
Received 25 November 2003. Accepted in revised form 20 April 2004
Key words: Climate change, crought, Mediterranean ecosystems, mineralomasses, Quercus ilex, soil, nutrient
concentrations, nutrient cycles, phosphorus
Abstract
Mediterranean ecosystems are water-limited and frequently also nutrient-limited. We aimed to investigate the
effects of increasing drought, as predicted by GCM and eco-physiological models for the next decades, on the
P cycle and P plant availability in a Mediterranean forest. We conducted a field experiment in a mature evergreen
oak forest, establishing four drought-treatment plots and four control plots (150 m2 each). After three years, the
runoff and rainfall exclusion reduced an overall 22% the soil moisture, and the runoff exclusion alone reduced it
10%. The reduction of 22% in soil moisture produced a decrease of 40% of the accumulated aboveground plant
P content, above all because there was a smaller increase in aerial biomass. The plant leaf P content increased by
100 ± 40 mg m−2 in the control plots, whereas it decreased by 40 ± 40 mg m−2 in the drought plots. The soil
Po-NaHCO3 (organic labile-P fraction) increased by 25% in consonance with the increase in litterfall, while the
inorganic labile-P fraction decreased in relation to the organic labile-P fraction up to 48%, indicating a decrease in
microbial activity. Thus, after just three years of slight drought, a clear trend towards an accumulation of P in the
soil and towards a decrease of P in the stand biomass was observed. The P accumulation in the soil in the drought
plots was mainly in forms that were not directly available to plants. These indirect effects of drought including the
decrease in plant P availability, may become a serious constraint for plant growth and therefore may have a serious
effect on ecosystem performance.
Introduction
In Mediterranean ecosystems the most serious effects
of climate change (IPCC2001) may well be those
which are related to increased drought, since water
stress is already the principal constraint in Mediterranean areas (Specht, 1979; Mooney, 1989). Over the
last century in the Mediterranean region, temperatures
have shown an overall trend towards warming (Kutiel
and Maheras, 1998; Piñol et al., 1998; Peñuelas et al.,
2002). Precipitation has either exhibited a long-term
downward trend, principally in the dry season (Maheras, 1988; Kutiel et al., 1996; Esteban-Parra et al.,
1998), or no significant change at all (Piñol et al.,
∗ FAX No: 93 581 41 51. E-mail: [email protected].
1998; Peñuelas et al., 2002), even though in all cases
a rise in the evapotranspiration potential has led to
increased aridity. The decline in total rainfall and/or
soil water availability expected for the next decades
(IPCC, 2001) may turn out to be even more drastic
under warmer conditions with a CO2 -rich atmosphere
and greater demand for water (Walker et al., 2000).
Nevertheless, water availability is not the only
limiting factor in Mediterranean ecosystems. Nutrient
supplies have often been shown to be an important factor in the growth, structure and distribution
of these communities (Kruger, 1979; Specht, 1979;
Carreira et al., 1992; Sardans, 1997; Henkin et al.,
1998). Mediterranean soils often suffer from nutrient
deficiencies (Specht, 1973; Kruger, 1979; Terradas,
2001), which can be worsened by climate change.
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Along with nitrogen, phosphorus is a frequent limiting factor in Mediterranean ecosystems (Zinke, 1973;
Sardans, 1997, Henkin et al., 1998; Hanley and Fenner, 2001). In these Mediterranean ecosystems, the
effects of climate change on plant growth and nutrient cycles could be linked to the availability of this
particular nutrient (Deacon, 1983; Minerbi, 1987).
The effects of climate change on nutrient supply
in Mediterranean areas may depend on a trade-off
between warming and the effects of drought. Nutrient biomass concentration results from the balance of
nutrient uptake and growth. Nutrient uptake could be
increased by warming, given that decomposition and
mineralization rates are increased (Anderson, 1991;
Rustad et al., 2001). However, if growth also increases, leaf nutrient concentrations may not increase
since the nutrients will be diluted into greater biomass.
Additionally, higher temperatures also encourage microbial metabolism, which in turn increases nutrient
sequestration by soil microbes. As a result, the amount
of available nutrients for plants may decrease (Jonasson et al., 1993). On the other hand, in these waterlimited ecosystems, increased temperatures will further decrease soil water-availability (Larcher, 2000),
which will very likely result in a decrease in nutrient
uptake by roots and in the movement of these nutrients to shoots (Bradford and Hsiao, 1982), and act as
an obstacle to microbial activity. Nevertheless, even
if nutrient uptake is decreased and growth is reduced,
leaf nutrient concentration may not decrease owing to
the concentration effect.
Sclerophylly is a typical Mediterranean trait that
is usually increased when the environment evolves towards drier conditions (Smith and Nobel, 1977; Dunn
et al., 1977; Sabaté et al., 1992; Oliveira et al., 1994).
Sclerophyllous leaves are rich in structural compounds
(Rundel, 1982; Gallardo and Merino, 1992; Turner,
1994a, b) and the greater nutrient reabsorption rates
typical of Mediterranean plants (Monk, 1966; Grubb,
1977; Gallardo and Merino, 1992), along with other
sclerophyllous traits, can decrease litter decomposition rates, which can then lead to more occluded humic
compounds retaining nutrients in non-available forms
in the soil. Conversely, a reduction in nutrient losses
in litterfall could be a strategy employed by sclerophyllous plants adapted to poor soils (Aerts, 1995)
and could partially compensate for decreased nutrient
uptake in dry conditions. The quality of soil organic
matter has a significant effect on litter decomposition
rates (Pastor et al., 1984; Coûteaux et al., 2002). On
the other hand, microbial activity has been correlated
with soil moisture. Drier climatic conditions decrease
microbial enzyme activity (Boissier and Fontvielle,
1995; Pulleman and Tietema, 1999; Li and Sarah,
2003), which is usually optimal at intermediate to high
levels of soil moisture (Zaman et al., 1999).
We hypothesised that an increase in the water
deficit in a Mediterranean ecosystem, as forecasted
for the coming decades by GCM (IPCC, 2001) and
by eco-physiological models such as Gotilwa (Gracia
et al., 1999), would decrease P soil availability for
plants and therefore the P accumulated in the aboveground biomass. Instead, there would be an increase
in the concentration of the non-directly available Pfractions in the soil as a result of a decrease in soil
mineralization rates.
To test these hypotheses, we conducted a threeyear field experiment in a mature Mediterranean evergreen holm oak forest where we simulated the drought
predicted by GCM and eco-physiological models for
the next decades. We investigated the impacts of this
experimental decline in soil moisture on: (i) soil P
fractions, including those available for plants, and
(ii) the concentrations and contents of P in biomass
and litter.
Material and methods
Study site
The study was carried out on a south-facing slope
(25%) in a natural holm oak forest in the Prades mountains in southern Catalonia (41◦13 N, 0◦ 55 E). The
soil consists of a stony xerochrept on a bedrock of
metamorphic sandstone with a depth ranging between
35 and 90 cm. The average annual temperature is
12 ◦ C and the average annual rainfall is 658 mm. The
summer drought is pronounced and usually lasts for
three months. The vegetation consists of a dense forest
dominated by Quercus ilex with abundant Phillyrea
latifolia, Arbutus unedo and other evergreen species
well-adapted to drought conditions (Erica arborea,
L. Juniperus oxycedrus L., Cistus albidus L.), and
the occasional individual of deciduous species (Sorbus
torminalis L. Crantz and Acer monspessulanum L.).
Experimental design
Eight 15 × 10 m plots were delimited at the same
altitude along the slope. Half of the plots received the
drought treatment and the other half were designated
as control plots. The drought treatment consisted of
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partial rain exclusion carried out by suspending PVC
strips and funnels at a height of 0.5–0.8 m above the
soil surface. Strips and funnels covered approximately
30% of the total plot surface. A ca. 0.8 m-deep ditch
was excavated along the entire top edge of the upper
part of the treatment plots to intercept runoff water,
and all water intercepted by strips, funnels and ditches
was conducted to below the bottom edge of the plots.
This drought treatment has been applied since 1999.
Sampling and soil analysis
Soil moisture was measured every fifteen days
throughout the three years of the experiment by Time
Domain Reflectometry (Tektronic 1502C, Beaverton,
OR, USA) (Zegelin et al., 1989). Three stainless steel
cylindrical rods, 25 cm long, were driven into the soil
at four randomly selected places in each plot and a
time domain reflectometer was connected to the ends
of the rods for each measurement.
In March 2002 (three years after the treatment was
first applied) the soils of all the different plots were
sampled to analyse the different fractions of P in the
soil. Four soil cores (20 cm deep) were randomly collected from every control plot (Control samples, C).
In the drought plots, four soil cores (20 cm deep) were
randomly collected in each plot from in between the
cover provided by the plastic strips (Drought samples,
D), and then four further soil cores (20 cm deep) were
randomly collected from below the plastic strips (DD
samples). In this way we analysed the effects of three
different water supply levels: Control (C), affected
by runoff exclusion (D), and affected by both rainfall
exclusion and runoff exclusion (DD).
Phosphorus was extracted using a modified sequential Hedley fractionation method (Tiessen et al.,
1984; Tiessen and Moir, 1993). A 2 g soil sample
was placed in a 50 mL plastic centrifuge tube and its
labile-P was extracted with 30 mL of 0.5 M Na HCO3
(pH 8.5) (bicarbonate-extractable P fraction). With the
remaining soil sample, this process was repeated with
increasingly stronger reagents to remove the more
tightly bound P. We used 0.1 M Na OH (Hydroxideextractable P fraction), 1 M HCl (HCl-extractable P
fraction), 10 M cHCl (concentrated HCl-extractable
P fraction) and H2 SO4 -H2 O2 (residual P fraction)
(Taranto et al., 2000). The NaHCO3 , NaOH and cHCl
extracts were divided and half of the sample was digested with H2 SO4 -H2 O2 in order to determine the total
P. For these extracts, the organic P (Po) was calculated
by the subtraction of each inorganic P fraction (Pi)
from the respective total P fraction. All extracts were
analysed for orthophosphate by the Vanade Molybdate
method.
Correspondence between current and traditional
terminology – labile, not occluded, occluded and residual – is discussed by Cros and Schlesinger (1995).
Extraction with bicarbonate is thought to simulate the
action of plant roots when dissolving P minerals and
also to give an indication of plant-available P (Olsen
et al., 1954) and the P-inorganic forms which are easily dissolved from solid phases in the soil (Tiessen
and Moir, 1993). These are the P forms considered to
be plant-available and microbe-available in the shortterm. The hydroxide-P extract is thought to remove
P that is associated with the surface of amorphous
and some crystalline Al and Fe minerals. It is probably available in the mid-term. The organic P (Po) in
the bicarbonate extract is thought to be derived from
organic compounds that are readily mineralized by microbes, while Po in the hydroxide extract represents
more stable P that is involved in the mid-term P transformation in soils. The remaining P extracts (HCl,
cHCl and H2 SO4 -H2 O2 ) represent P that is available
over long-term periods (Cros and Schlesinger, 1995).
The HCl fraction represents P associated with calcium
carbonate minerals; the cHCl extract removes the Pi
and Po that is bound to the interior of Fe and Al minerals and apatite (Tiessen and Moir, 1993). The residual
P represents the most stable form of P, only available
in the long-term, if at all (Cros and Schlesinger, 1995).
Sampling and analysis of P in biomass and in
litterfall
The leaves, stems and litterfall of Quercus ilex were
sampled and analysed in March 1999 and March 2002.
Quercus ilex roots were sampled in March 2002. On
the basis of the P biomass concentrations and the estimation of total aerial biomass carried out on the same
dates (Ogaya et al., 2003), we calculated the total
amount of P in the aerial biomass and the total gains
of P in the biomass over the three-year period in the
control and drought plots.
Quercus ilex constitutes the greatest part of the plot
biomass. For this reason, the biomass sampling conducted in this species was taken to be representative of
the full biomass of the stand. Four samples of leaves,
fine roots (φ < 5 mm), thick roots (φ > 5 mm),
fine stems (φ < 10 mm), thick stems (φ > 10 mm)
and litterfall were randomly sampled in each plot. The
litterfall was collected in 20 circular baskets (of 27 cm
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diameter with a 1.5 mm mesh) randomly distributed
on the ground in each of the eight plots. Leaf litter dry
weight was measured after drying in a oven at 70 ◦ C
until constant weight.
The biomass samples were dried at 70 ◦ C for
48 h and then ground in a FRITSCH pulverisette
09202 (Laval Lab Inc. Laval, Canada). To analyse
the P biomass concentrations, we conducted an ACPIES (Atomic Emission Spectroscopy with Inductively
Coupled Plasma) analysis with a previous biacid digestion (nitric:percloric, 2:1) in a microwave oven
(Samsung) The ACP-IES analyses were conducted in
a JOBIN YBON JI 38 spectrophotometer (Jobin Ybon,
Ybon, France).
Statistical analyses
The effects of the drought treatment on each studied variable were investigated by means of ANOVA
analyses. A post-hoc test (Bonferroni/Dunn) was also
conducted to compare results from the different levels
of drought treatment. These analyses were conducted
with the Statview 5.01 programme (Abacus Concepts,
1992, SAS Institute Inc. Berkeley Ca, USA).
Results
P in the Soil
During the overall drought experiment the moisture of
the soil from between the plastic strips in the drought
plots (D) decreased on average by 10% in relation to
the soil from control plots (23.5 ± 0.6% in D versus
26.1 ± 0.4 in C, P < 0.0001). The moisture of the soil
below the plastic strips in the drought plots (DD) decreased on average by 21.8% in relation to the control
plot soils (P < 0.0001). The overall decrease in soil
moisture in the drought plots was 15% (P < 0.01).
The soil moisture of the C soils was 21.5 ± 1% , of
the D soils was 19.6 ± 2% and of the DD soils was
18 ± 2% in the sampling day.
The total labile-P (NaHCO3 extract) was 43%
higher in the below-strips (DD) samples than in the
control samples (P < 0.0001) (Figure 1). Similar
results were found for the labile-Po (Figure 1). In contrast, the highest Pi labile concentrations were found
in the control (C) soil samples, although the differences with regard to DD and D soil samples were not
statistically significant (Figure 1). These labile-Pi fraction concentrations were much lower than those of the
Figure 1. Labile-P soil concentration fractions (mg P g−1 soil) in
the control plots (C) and in the treatment plots, in between strips
(D), i.e. affected by runoff exclusion (10% less soil water) and below
strips (DD), i.e. affected by runoff exclusion (22% less soil water).
Error bars are standard errors (n = 4 plot averages of 4 samples per
plot). Statistically significant differences (P < 0.05) between the
three types of treatments are indicated by different letters.
labile-Po fraction in all the different types of treatment
(ca. 0.02 vs. ca. 1 mg g−1 ; Figure 1).
The total P-NaOH extract fraction was significantly higher in the D soil samples than in the C
samples (P < 0.05). This difference was similar
to that found in the organic Po-NaOH extract fraction (P < 0.05) (Figure 2). Although there were no
significant differences among treatments in the concentration of the Pi-NaOH fraction, as in the labile-Pi
fraction, it also tended to be smaller in the drought
treatments (Figure 2). The concentration values of the
Pi-NaOH fraction were much lower than those of the
Po-NaOH fraction in all the different treatment types
(ca. 0.08 vs. ca. 0.6 mg g−1 ; Figure 2).
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Figure 2. Mid-term P soil concentration fractions (mg P g−1 soil)
in the control plots (C) and in the treatment plots, in between strips
(D), i.e. affected by runoff exclusion (10% less soil water) and below
strips (DD), i.e. affected by runoff exclusion (22% less soil water).
Error bars are standard errors (n = 4 plot averages of 4 samples per
plot). Statistically significant differences (P < 0.05) between the
three treatments are indicated by different letters.
The soil concentrations of the P-HCl fraction (P
associated with calcium carbonate mineral; available
in the long-term) were significantly higher in the D
soil plot samples than in the C samples (P = 0.017).
The concentrations in the C soil samples were also
lower than those of the DD samples, although in this
case the differences were not statistically significant
(Figure 3). The total soil concentration values of the
P-cHCl fraction (P available only in the long-term)
and the organic Po-cHCl (organic P bound in the interior of Fe and Al minerals and apatite) were higher
in the C than in the D and the DD (P < 0.0001)
soil plot samples (Figure 3). The concentrations of the
Figure 3. Long-term P soil concentration fraction (mg P g−1 soil)
in the control plots (C) and in the treatment plots, in between strips
(D), i.e. affected by runoff exclusion (10% less soil water) and below
strips (DD), i.e. affected by runoff exclusion (22% less soil water).
Error bars are standard errors (n = 4 plot averages of 4 samples per
plot). Statistically significant differences (P < 0.05) between the
three soil sample types are indicated by different letters.
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inorganic Pi-cHCl fraction were not statistically different between different types of treatments (Figure 3).
Concentrations in inorganic and organic P-cHCl soil
fractions were similar (ca. 0.2 mg g−1 ; Figure 3). No
significant differences were found for concentrations
of the P-H2 SO4 -H2 O2 fraction (stable and recalcitrant
P-soil fraction) (Figure 3).
The total Po (PoT = Po-NaHCO3 + Po-NaOH +
Po-cHCl) soil concentrations were slightly lower, although not significantly, in the C plot soils (1.575 ±
0.089 mg g−1 ) than in the D (1.786 ± 0.110 mg g−1 )
and DD plot soils (1.717 ± 0.096 mg g−1 ). The
total P content (Pi + Po) was significantly lower in
the C soils (2.230 ± 0.089 mg g−1 ) than in the D
soils (2.522 ± 0.106 mg g−1 , P = 0.025), and also
lower, but not significantly so, than in the DD soils
(2.349 ± 0.096 mg g−1 , P = 0.14).
We used the ratio Pi/Po of the NaHCO3 extract
to evaluate the effects of the different treatments on
the mineralization capacity of the soil, given that the
NaHCO3 fraction is the directly available P source
used by soil micro-organisms. Our analyses showed
the significant effects of the drought treatment. The
lower water availability decreased the Pi (mineralized P) with regard to the Po (non-mineralized P).
This effect was marginally significant (P = 0.089)
when comparing soils from control plots with soils
in drought plots from between the plastic strips (affected by runoff exclusion), but clearly significant
(P = 0.014) when comparing control soils with soils
from below the plastic strips (affected by both runoff
and rainfall exclusion) which decreased 48% the ratio
Pi/Po (Figure 4).
P in Quercus ilex trees
The P concentration in leaves, fine stems, thick stems
and litterfall (data not shown), and the total P in stand
biomass per plot unit area at the beginning of the
experiment (March 1999) (Table 1) were not significantly different in the drought plots when compared
with the control plots. After three years of treatment,
the P concentrations in the different plant fractions in
the control plots and in the drought plots were still
not significantly different except for those of the fine
roots, which were lower in the drought plots than in
the control plots (Figure 5).
Foliar P content significantly increased by 100 mg
P m−2 in the control plots, but decreased by 40 mg P
m−2 in the drought plots (Figure 6). In contrast,
the litterfall P content increased more in the drought
Figure 4. Pi/Po ratio of the labile-P soil fraction (NaHCO3 extraction) in the control plots (C) and in the treatment plots, in between
strips (D), i.e. affected by runoff exclusion (10% less soil water)
and below strips (DD), i.e. affected by runoff exclusion (22% less
soil water). Error bars are standard errors (n = 4 plot averages of 4
samples per plot). Statistically significant differences (P < 0.05)
between the three types of treatments are indicated by different
letters.
Figure 5. P concentrations: (mg P g−1 ) (Mean ± S.E.) of leaves,
fine stems (φ < 10 mm), thick stems (φ > 10 mm), fine roots
(φ < 0.05 mm), thick roots (φ > 0.05 mm) and litterfall of Quercus ilex sampled in March 2002. These results were analysed by
a one-way ANOVA. (∗ ) P < 0.1 between two treatment stands
(control and drought).
plots 27 ± 7 mg m−2 ) than in the control plots (5 ±
7 mg m−2 ) (Figure 6, Table 1).
Discussion
Mediterranean traits
The leaf-P concentrations in Quercus ilex in the control plots, 0.93 ± 0.032 mg g−1 , are similar to those
reported for this species in other Mediterranean areas
(Canadell and Vilà, 1992; Castro-Díez et al., 1997).
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Table 1. P content (g m−2 ) (Mean ± S.E.) in leaves, fine stems (φ < 10 mm),
thick stems (φ > 10 mm), total aerial biomass and litterfall of Quercus ilex
trees in a forest in the Prades mountains in March 1999 and March 2002. The
changes produced after these three-year periods are also presented. The results
were analysed by a one-way ANOVA. P = Statistical significance of the difference between control and drought plots. Significant differences are highlighted
in bold type
1999 sample
Biomass fraction
Leaves
Fine stems
Thick stems
Aboveground biomass
Litterfall
Control Plots
0.436 ± 0.04
2.03 ± 0.25
6.09 ± 0.68
8.63 ± 0.2
0.069 ± 0.007
Drought Plots
0.632 ± 0.1
2.013 ± 0.25
6.65 ± 0.85
9.27 ± 0.2
0.076 ± 0.01
P
0.18
0.97
0.80
0.1
0.5307
Control Plots
0.54 ± 0.06
1.6 ± 0.2
9.6 ± 1.6
11.7 ± 1.8
0.064 ± 0.011
Drought Plots
0.59 ± 0.07
1.7 ± 1.0
8.5 ± 1.2
10.9 ± 1.5
0.049 ± 0.008
P
0.6
0.54
0.61
0.73
0.3161
Control Plots
0.1 ± 0.04
−0.47 ± 0.1
3.49 ± 1.6
2.97 ± 1.56
0.005 ± 0.007
Drought Plots
−0.04 ± 0.04
−0.28 ± 0.13
1.89 ± 1.22
1.55 ± 1.30
0.027 ± 0.007
P
0.019
0.26
0.43
0.49
0.045
2002 sample
Biomass fraction
Leaves
Fine stems
Thick stems
Aboveground biomass
Litterfall
2002–1999 increments.
Biomass fraction
Leaves
Fine stems
Thick stems
Aboveground biomass
Litterfall
The total P content in the Quercus ilex biomass of the
control plots (2.97 g P m−2 ) is similar to the 2.57–
4.57 g P m−2 reported by Santa Regina (2000) in
Quercus pyrenaica stands in Spain. In other Quercus
ilex stands near our experimental stands, Escarré et al.
(1999) reported 7.7 g P m−2 . However, these stands
were sited on a NW-facing slope and the measurements also took into account the shrub and accompanying trees. The total P content of the first 25 cm of
the soil profile (1.80 to 2.20 mg P g−1 of soil) is relatively high in comparison with other soils from other
regions in the world (Kramer and Green, 1999; Lilienfein et al., 2000; Turrion et al., 2000; Schlichting et al.,
2002), and in the Mediterranean context would be in
the high range of P content (Bonifacio et al., 1998).
Thus the traits of the holm oak forest we studied reveal
it to be a typical Mediterranean forest.
These Prades soils are fairly rich in total P, but only
contain moderate amounts (0.014 to 0.024 mg P g−1
of soil) of assimilable-P (NaHCO3 -Pi). Two factors
indicate that these soils accumulate P in non-directly
available forms, probably as a result of the water deficit: the total Po is clearly higher than the total Pi
and the mid-term and long-term assimilable-P forms
present higher concentration values than the shortterm assimilable-P soil fractions in the studied upper 25 cm of the soil profile. The high Po fraction
(between 80–85% of the total P-soil) may be due, at
least in part, to the high levels of organic matter found
in these Mediterranean forests, where low mineralization rates are caused by low water availability and
litterfall of poor nutritional quality.
The effects of drought enhancement
After three years of drought treatment, the immediate and mid-term assimilable-Po soil fractions increased significantly in the drought plots, mainly as
374
Figure 6. Changes in the foliar P content, the total aboveground P
content and the litterfall P content after three years (2002–1999) of
experimental drought. Errors bars are standard errors (n = 4 plot
averages of 5 samples per plot). Statistically significant differences
(P < 0.05) between the control and drought stands are indicated by
different letters.
a consequence of the increase in litterfall (Ogaya and
Peñuelas, 2003). On the other hand, the corresponding
Pi fractions decreased. Thus, the drought treatment decreased the soil concentrations of P directly available
to plants. However, as expected, given the relatively
short duration of the treatment (3 years), the drought
treatment did not have clear effects on the more occluded fractions (extract with HCl, cHCl, H2 SO4 H2 O2 ). Summarising, the drought treatment induced
an increase in the litterfall production that in turn increased the short-term and mid-term availability of
Po forms for microbe mineralization, although the Pi
forms of these fractions were lower in the soils of the
drought-treatment plots, a result which indicates that
slower microbe mineralization took place, probably
due to lower water availability. Soil enzyme activity,
and particularly soil phosphatases activity, has been
shown to decrease in response to drought enhancement
in semiarid soils (Kramer and Green, 2000) and in
Mediterranean soils (Li and Sarah, 2003).
The decrease in P-available forms and the increase
in the P-occluded soil fraction will reduce the P uptake
and consequently will induce lower foliar P contents.
After three years of drought treatment, all the results
point towards a lower accumulation of P in the stand
biomass, in great part due to decreased biomass accumulation. The decreases in total plant P contents are
also partly due to the increase in the P loss in the stand
biomass and to slower mineralization rates, probably
as a consequence of the effect of water deficit on enzyme activity. The decrease in P concentrations was
greater in the fine stems, probably as a consequence of
higher P allocation to photosynthetic structures aimed
at optimising resources and avoiding a decrease in the
photosynthetic capacity caused by a deficient nutrient
supply and the consequent reduction in the amount of
photosynthetic enzymes. A great continuous reduction in precipitation in the Alto Adagio (Italy) was
also associated to an increase in identified nutrient
deficiencies in tree foliage resulting from the immobilization of nutrients in soil in response to the increasing
drought (Minerbi, 1987).
Availability patterns over time of rock-derived elements such as P show a decline when ecosystems
reach maturity (Chadwick et al., 1999). This pattern
may be accelerated in the forecasted drier conditions
in the Mediterranean region by the increase in unavailable P in soil fractions and the increase of losses after
rewetting episodes through drought periods (Pulleman
and Tietema, 1999; Turner and Haygarth, 2001; Baum
et al., 2003). Moreover, an increase in P accumulation
in soil could lead to a P loss in Mediterranean ecosystems after torrential rainfall and erosive processes,
which have been shown to be already a problem
in Mediterranean ecosystems (Thomas et al., 1999).
The subsequent lack of P could then hamper photosynthetic activity and the water-use efficiency of the
remaining plant biomass. Furthermore, other negative
and indirect effect of drought on soil enzyme activity
in the Mediterranean region is the results from the decrease in plant cover as a consequence the enhanced
drought (Garcia et al., 2002).
Currently, P is probably not yet a limiting factor
in this studied Mediterranean ecosystem, although in
the mid- and long-terms the decrease in P in the stand
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biomass, the increase in P in soil principally in nonavailable forms, and the increase in losses through
rewetting episodes and torrential rainfall under a more
irregular climatic regime may well hinder the supply of P to plants, thereby further aggravating the
stress produced by water shortages. All these factors
together would accelerate the degradation of Mediterranean forests and their substitution by other less
water- and nutrient-demanding communities such as
Mediterranean shrublands. These results constitute a
clear example of the indirect synergic effects of increased drought on other environmental stress-factors
such as nutrient shortages. They must be taken into
account in the study of the impact of climate change.
Acknowledgements
We are grateful to the Departament d’Agricultura,
Ramaderia i Pesca of the Generalitat de Catalunya
(the Catalan Ministry of Agriculture, Livestock and
Fisheries of the Autonomous Government of Catalonia) and A. Vallvey for permission and help in
conducting this research in the Poblet Forest. We
also wish to thank R. Ogaya for his technical assistance. This research was supported by MCYT (Spanish Government) projects REN2001-0003/GLO and
REN 2003-04871/GLO, and the EU project VULCAN
(EVK2-2000-0094).
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Section editor: M. A. Adams