Functional
Ecology 2007
21, 191–201
Drought changes phosphorus and potassium accumulation
patterns in an evergreen Mediterranean forest
Blackwell Publishing Ltd
J. SARDANS† and J. PEÑUELAS
Unitat d’Ecofisiologia CSIC-CEAB-CREAF. CREAF (Centre de Recerca Ecològica i Aplicacions Forestals) Edifici C,
Universitat Autònoma Barcelona, 08193 Bellaterra (Barcelona), Spain
Summary
1. Climate models predict more extreme weather in Mediterranean ecosystems, with
more frequent drought periods and torrential rainfall. These expected changes may
affect major process in ecosystems such as mineral cycling. However, there is a lack of
experimental data regarding the effects of prolonged drought on nutrient cycling and
content in Mediterranean ecosystems.
2. A 6-year drought manipulation experiment was conducted in a Quercus ilex Mediterranean forest. The aim was to investigate the effects of drought conditions expected
to occur over the coming decades, on the contents and concentrations of phosphorus
(P) and potassium (K) in stand biomass, and P and K content and availability in soils.
3. Drought (an average reduction of 15% in soil moisture) increased P leaf concentration by 18·2% and reduced P wood and root concentrations (30·9% and 39·8%, respectively) in the dominant tree species Quercus ilex, suggesting a process of mobilization
of P from wood towards leaves. The decrease in P wood concentrations in Quercus ilex,
together with a decrease in forest biomass growth, led to an overall decrease (by
approximately one-third) of the total P content in above-ground biomass. In control
plots, the total P content in the above-ground biomass increased 54 kg ha−1 from 1999
to 2005, whereas in drought plots there was no increase in P levels in above-ground
biomass. Drought had no effects on either K above-ground contents or concentrations.
4. Drought increased total soil soluble P by increasing soil soluble organic P, which is
the soil soluble P not directly available to plant capture. Drought reduced the ratio of
soil soluble inorganic P : soil soluble organic P by 50% showing a decrease of inorganic
P release from P bound to organic matter. Drought increased by 10% the total K content
in the soil, but reduced the soil soluble K by 20·4%.
5. Drought led to diminished plant uptake of mineral nutrients and to greater recalcitrance of minerals in soil. This will lead to a reduction in P and K in the ecosystem, due
to losses in P and K through leaching and erosion, if the heavy rainfalls predicted by
IPCC (Intergovernmental Panel on Climate Change) models occur. As P is currently a
limiting factor in many Mediterranean terrestrial ecosystems, and given that P and K
are necessary for high water-use efficiency and stomata control, the negative effects of
drought on P and K content in the ecosystem may well have additional indirect negative
effects on plant fitness.
Key-words: Arbutus unedo, biomass, climate change, drought, nutrient content, Phillyrea latifolia, phosphorus,
potassium, Quercus ilex, soil
Functional Ecology (2007) 21, 191–201
doi: 10.1111/j.1365-2435.2007.01247.x
Introduction
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society
Water is the most important limiting factor in Mediterranean ecosystems. In these ecosystems, aridity has
increased in recent decades (Piñol, Terradas & Lloret
†Author to whom correspondence should be addressed.
E-mail: [email protected]
1998; Peñuelas, Filella & Comas 2002) and both Global
Circulation (Houghton et al. 2001) and ecophysiological models predict greater levels of drought in the near
future: for example, GOTILWA (Growth Of Trees Is
Limited by Water) predicts a decrease of 25% in soil
moisture between 2000 and 2040 (Sabaté, Gracia &
Sánchez 2002; Peñuelas et al. 2005). Furthermore, more
intense and more frequent dry periods are expected
191
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J. Sardans &
J. Peñuelas
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
to occur along with ever heavier torrential rainfall
(Houghton et al. 2001). All this will affect nutrient
cycling and losses, two highly significant processes in
Mediterranean ecosystems in which nutrients such as
nitrogen and phosphorus (P) are often limiting factors
(Kruger 1979; Henkin et al. 1998; Sardans, Rodà &
Peñuelas 2004, 2005a; Sardans, Peñuelas & Rodà 2006a)
in spite of the fact that human activities may increase
their inputs to the ecosystems (Peñuelas & Filella 2001).
Observational and experimental evidence supports
the assumption that water stress affects nutrient levels
in trees (Escudero et al. 1992; Clancy, Warner & Reich
1995; Díaz & Roldan 2000). Of the different nutrients
involved, P and potassium (K) tissue concentrations play
very important roles in plant biology (Sundareshwar
et al. 2003; Wissuwa 2003; Paoli, Curran & Zak 2005)
and their availability has been reported to be inversely
correlated with water availability (Kemp & Moody
1984; Díaz & Roldan 2000).
A decrease in soil moisture may have a negative effect
on soil microbial activity (Sardans & Peñuelas 2005) and
as sclerophylly usually increases when the environment
evolves towards drier conditions (Sabaté, Calvet & Gracia
1992; Oliveira et al. 1994; Sardans, Peñuelas & Rodà
2006b), the resulting accumulation of recalcitrant organic
matter in soil may slow down organic matter decomposition (Pastor et al. 1984; Coûteaux, Aloui & KurzBesson 2002). Previous work has shown a decrease in
soil soluble P as a consequence of drought in Mediterranean forests (Sardans & Peñuelas 2004).
Drought can reduce the P and /or K contents in stand
biomass by reducing soil mineralization rates (Sardans
& Peñuelas 2005) and plant absorption capacity and/
or growth, resulting in an accumulation of P and K
nonavailable forms, in soil and plant litter. If plant P
and K contents are reduced and soil P and K contents
are increased, the risk of P and K losses given that
IPCC (Intergovernmental Panel on Climate Change)
models predict an increase in torrential rainfall in the
Mediterranean Basin (Houghton et al. 2001) and thus
greater soil erosion (De Luis, González-Hidalgo &
Raventós 2003). If drought affects P and K cycling and
availability, a strong synergic effect will result as P
availability has a positive effect on water-use efficiency
(Sing et al. 2000; Ruiz-Lozano et al. 2001; Mohammad
& Zuraigi 2003; Sardans, Peñuelas & Rodà 2005b) and
K is particularly important in dry environments due to
its role in stomata control and leaf water loss. These
indirect effects of drought on P and K availability and
content in different ecosystems compartments, in the
mid- and long-term (the coming decades), still need to
be investigated further in order to fully understand the
overall effect of the drought predicted by IPCC models.
Nevertheless, to our knowledge, no field experiment in
the Mediterranean Basin has ever studied the effects of
drought on P and /or K contents at a ecosystem level.
To investigate the effects of drought on P and K
dynamic patterns in an evergreen Mediterranean forest,
a 6-year field experiment was conducted in a holm oak
Quercus ilex forest by means of a simulation of the
drought levels predicted by GCM and ecophysiological
models for the next decades (Houghton et al. 2001;
Sabaté et al. 2002; Peñuelas et al. 2005). We investigated
the impacts of this experimental decrease of soil
moisture on: (1) P and K concentrations and contents
in the biomass (leaf, wood, root and litter) of the three
dominant species in the ecosystem, and (2) on the concentrations of total and available forms of soil P and K.
Materials and methods
field site
The study was carried out in a natural Quercus ilex oak
forest in the Prades mountains in southern Catalonia
(north-east Spain) (41°13′ N, 0°55′ E) on a south-facing
slope (25%). The soil is a stony Dystric Xerochrept
(Soil Survey Staff 1999) lying on a bedrock of metamorphic sandstone. Its depth ranges between 35 and
100 cm, with the depth of Horizon A ranging between
25 and 30 cm. The average annual temperature is 12 °C
and an average rainfall of 658 mm, with a period between
September to November experiencing the maximum
of rainfall. Summer drought is pronounced and usually lasts for 3 months. The vegetation consists of a
dense forest with a canopy height average of 8–10 m
dominated by Quercus ilex L. (20·8 m2 ha−1 of trunk
basal area at 50 cm of height) accompanied by abundant Phillyrea latifolia (7·7 m2 ha−1 of trunk basal area
at 50 cm of height and Arbutus unedo L. A number of
other evergreen species well-adapted to drought conditions such as Erica arborea L., Junniperus oxycedrus
L., Cistus albidus L., and occasional individuals of
deciduous species such as Sorbus torminalis L. Crantz
and Acer monspessulanum L. are also present. In winter
1999, the above-ground biomass (AB) of Quercus ilex
represented 77·1% of the total biomass, while Phillyrea
latifolia represented 12·6% and Arbutus unedo 7·8%;
the sum of the aerial biomass of these three species
thus represented 97·6% of the whole ecosystem AB.
In the winter of 2005, the biomass for the same three
species were 75·6%, 13·3% and 8·7%, respectively,
representing in total a 97·6% of the total AB.
experimental design
Eight 15 × 10 m plots were established at the same
altitude (930 m above sea level) on a slope. Four of the
plots received the drought treatment and four plots left
as controls. All the plots were established in an area
with the same aspect and altitudinal level, with a minimum distance between plots of 15 m. The treatments
were randomly assigned to different plots. The drought
treatment consisted of partial rainfall exclusion by
suspending transparent PVC strips at a height of 0·5–
0·8 m above soil level and covered approximately 30%
of the total soil surface. Four plastic strips 14 m long
and 1 m wide were placed along the drought treatment
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Drought changes
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accumulation
patterns
plots and a 0·8 –1 m deep ditch was dug along the entire
top edge of the upper part of the treatment plots to
intercept runoff water. The water intercepted by the
strips and ditches was channelled to the bottom edge
of the plots. The drought treatment began in March
1999 (Ogaya et al. 2003). Soil moisture content was
measured every 2 weeks throughout the experiment
period by time domain reflectometry (Tektronix 1502
C, Beaverton, OR, USA; Zegelin, White & Jenkins 1989).
Three stainless steel cylindrical rods, 25-cm long, were
driven into the soil at four randomly selected places in
each drought plot. The time domain reflectometer was
connected to the ends of the rods to determine the soil
moisture content.
biomass and litter determination
Just before the treatment was begun, all living stems of
the three dominant species with a diameter of over
2 cm at 0·5 m height above the ground were tagged and
their circumferences measured at 50 cm height with a
metric tape. In January 2005, the circumferences of the
stems were measured again to calculate the annual
stem diameter increment.
Allometric relationships between above-ground tree
biomass and the diameter at 50 cm (D50) were calculated for Quecus ilex and Phillyrea latifolia in the studied
area (outside the plots). Total AB, leaf biomass (LB)
and stem biomass were measured by weighing plant
material after it had reached a constant weight in an
oven at 70 °C. The allometric relationships in Quercus
ilex (ln AB = 4·9 + 2·277 ln D50, r 2 = 0·98, n = 12) and
in Phillyrea latifolia (ln AB = 4·251 + 2·463 ln D50,
r2 = 0·97, n = 13) were used thereafter to estimate the
above-ground standing biomass of these two species in
the studied area (see Ogaya et al. 2003). To estimate
Arbutus unedo biomass, we used the allometric relationship (ln AB = 3·830 + 2·563 ln D50, r2 = 0·99, n = 10)
previously calculated in the same area by Lledó (1990).
LB was calculated by the following allometric relationships for Quercus ilex: ln LB = 3·48 + 1·70 ln D50,
r2 = 0·97, n = 12, for Phillyrea latifolia: ln LB = 1·43
+ 2·43 ln D50, r2 = 0·94, and for Arbutus unedo: ln
LB = 1·887 + 2·157 ln D50, r2 = 0·95. Stem biomass was
calculated by the difference between total AB and total LB.
Litterfall was collected in 20 circular baskets (27 cm
diameter with 1·5 mm mesh diameter) randomly distributed on the ground of each of the eight plots. The
fallen litter was collected every 15 days during 1999
and every 2 months during 2004. Total litterfall was
estimated by the proportion of the surface area of the
plots covered by the collecting baskets.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
biomass and soil sampling process
Prior to the start of the experiment (March 1999),
eight soil samples (four control plots and four drought
plots) were analysed to test the spatial variability of the
soils. There were no significant differences in P and K
availability and contents between control and drought
plots. In January 2005, just 6 years after the experiment
was initiated, all the soil and biomass samples were
collected, in order to evaluate the total contents in soil
and in stand biomass, at the same time. Eight samples
of leaf and stems from the three dominant species
(Quercus ilex, Phillyrea latifolia and Arbutus unedo)
were randomly sampled in each plot (four samples in
the sun and four samples in the shade). The leaves were
sampled from between 1·5 and 6 m where most foliar
biomass was located. Sample collection was standardized in order to avoid bias due to differences in the age
of tissues and their position with respect to sunlight.
The leaves sampled were those from current year leaves
of 1998 and 2004 and represented the majority of the
leaves of the plants of these three species. Stems were
collected separately and stems of 0·3–2 cm and more
than 2 cm in diameter were differentiated. We collected
four samples of each stem diameter class per plot. We
only sampled the trees and shrubs of the diameter class
between 2 and 12 cm of BD (at 5 cm), that represents
most of the community biomass (Ogaya et al. 2003;
Ogaya & Peñuelas 2007). The concentrations in the
stems of diameter 0·3–2 cm did not differ from those
with a diameter greater than 2 cm and thus only one
stem concentration was calculated for all stem diameters, which was taken as the wood concentration. All
leaves and stems were collected from different plants in
each plot. In 1999 and in 2005, five leaf litter samples
from each species (Quercus ilex, Phillyrea latifolia and
Arbutus unedo) from each plot, were analysed separately. The leaf litter that represented 87% of the total
litter mass, was analysed in the same way as the biomass.
We conducted the soil sampling in January 2005, i.e.
following 6 years of drought treatment. We randomly
sampled five cores from the first 30 cm of soil profile
(Horizon A) in control plots and 10 in each drought
plot. In the drought plots, we distinguished two levels
of drought: that of the soil between the strips (D) (runoff exclusion) and that under the strips (DD) (runoff
exclusion plus rainfall exclusion). We analysed these
two soil fractions separately because we had previously
observed that soil moisture decreased more under
plastic strips than between plastic strips, being the soil
moisture 27% lower under plastic strips than between
plastic strips in winter. Five soil cores were taken
between strips and five from under the strips, at a minimum distance of 1 m from the nearest tree or shrub;
in each control plot only five soil cores were randomly
sampled. We collected and analysed separately the 0–
15-cm deep soil and the 15–30-cm deep soil in each soil
core, as horizon A had an A1 subhorizon (first 15 cm)
rich in organic matter (7·25% W/W) and an A2 subhorizon (15–30 cm) with only moderate amounts of
organic matter (1·3% W/W). However, as extractable
soil P and K can have great variations through the year,
we conducted a seasonal study with additional samplings
in spring, summer and autumn in order to investigate
possible fluctuations in these variables.
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J. Sardans &
J. Peñuelas
Additionally five soil holes per plot under Quercus
ilex trees were dug and roots of this species were sampled (φ > 5 mm) in order to study the effects of drought
on root P and K concentration.
All the samples were taken to the laboratory and
stored at 4 °C until the analyses were carried out. In
order to analyse P and K in foliar tissues, leaves were
washed with distilled water as in Porter (1986).
For the analyses of total P and K, biomass and soil
samples were washed and dried in an oven at 60 °C
until constant weight was obtained. Then, they were
ground up in a CYCLOTEC 1093 (Foss Tecator,
Höganäs, Sweden) – in the case of the biomass samples
– or in a FRITSCH Pulverisette (Rudolstadt, Germany)
– in the case of the soils and bedrock samples.
P and K concentrations in all biomass and soil samples were measured using ICP-AES (Atomic Emission
Spectroscopy with Inductively Coupled Plasma) in a
JOBIN IBON JY 38 (Longjumeau, HORIBA Jobin
Ibon S.A.S., France). Before the biomass ICP-AES
analyses, an acid digestion of the 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 millilitres of the mixed acid
solution were added to 100 mg of dry biomass for each
sample. The digested solutions were brought to 10 mL
of final volume (HClO4 3%). During the acid digestion
process, two blank solutions (2 mL of acid mixture
without any sample biomass) were also analysed. In
order to assess the accuracy of digestion and analytical
procedures of biomasses, a standard certified biomass
(DC73351) was used.
For the determination of total P and K soil samples,
digestion was carried out in a microwave oven at 120 °C
for 8 h with 0·25 g of ground sample in 9 mL of HNO3
(65%) and 4 mL HF (40%) (Bargagli, Brown & Nelli
1995). The digested solutions were adjusted to 50 mL
final volume of HNO3 (3%), filtered with a Millex 0·45 µm
filter and stored at 4 °C until required. The analytical
precision for soil and bedrock analyses, as verified by
parallel analyses of international (GSR-6) standards,
was better than 5% for all trace elements analysed.
soil extract s
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
To determine the available P in soil, soluble Pinorganic
(Pi), an extraction with 0·5 m NaHCO3 was conducted.
We analysed the soil soluble Pi in 0·5 m NaHCO3 soil
extracts by the Olsen Method (Olsen et al. 1954). We
analysed Olsen-P soil fractions in the soil samples of
January 2005 and in order to detect possible annual
variations in Olsen-P fractions an additional soil
sampling and Olsen-P determination was conducted
in April 2005.
To determine total soil extractable P (Olsen-P), an
aliquot of the NaHCO3 extracts (3 mL) was digested
and analysed by the Olsen method (Olsen et al. 1954).
Soil extractable organic P (Olsen-Porganic) was determined
as the difference between total Olsen-P and Olsen-Pinorganic.
The extractable K fractions were analysed for each
soil sample. The K extracts were obtained by shaking
2 g of soil (or pulverized bedrock) with 12 mL of solvent (0·01 m NaNO3) as according to Yin et al. (2002)
and van Elteren & Budic (2004). The soil and the
0·01 m NaNO3 solvent were mixed in 50-mL plastic
centrifuge tubes and were used according to the method
given by Blaser et al. (2000). Two soil suspensions were
prepared for each sample. The soil mixtures were
equilibrated by shaking in a reciprocal shaker (100
strokes min−1) for 5 h, a technique based on batch
extraction studies by Gupta & Mackay (1966). After
equilibrium, soil solids were separated from the solution by centrifugation and then by filtration through a
0·45 µm pore-size membrane filter. The concentrations of K in the filtrates were determined as described
above for biomass and soil digests. In order to detect
possible annual variations in K concentrations in soil
extracts an additional soil sampling and K concentrations in soil extracts was conducted in April 2005.
statistical analyses
The effects of drought treatment on plant P and K concentrations and contents were investigated by t-test
using plot mean values of each variable. In the case of
soil P and K contents, we differentiated between soils
under plastic strips (runoff plus partial rainfall exclusion)
and soils between plastic strips (runoff exclusion). Thus,
for soil analyses we used an anova post-hoc test
(Bonferroni/ Dunn) to compare the three levels of water
availability (Control, D and DD). These analyses were
conducted with the statview 5·01 program (Abacus
Concepts, SAS Institute Inc., Berkeley, CA, USA).
Results
soil moisture
Between 1999 and 2005 the soil in drought treatment
plots submitted to runoff exclusion (D) had an average
soil moisture of 17·5% (SE = 0·5%, n = 100), 9% lower
than the soil from control plots, which had an average
soil moisture of 19·2% (SE = 0·5, n = 100) (anova,
F2,9 = 5·3, P = 0·03). The soil submitted to both runoff
and partial rainfall exclusion (DD) had an average soil
moisture of 15·4% (SE = 1·0, n = 100), 20% lower than
the soil from control plots (anova, F2,9 = 15·2, P = 0·002).
In the sampling data (January 2005), the decrease of
soil moisture was also more noticeable below plastic
strips (DD) than between plastic strips (D).
above-ground biomass accumulation
(1999 ‒ 2005)
Drought conditions had a tendency to reduce Quercus
ilex biomass accumulation (Table 1), while had no
effects on Phillyrea latifolia biomass accumulation
(Table 1). In Arbutus unedo, drought decreased the
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Drought changes
P and K
accumulation
patterns
Table 1. Above-ground biomass accumulation (kg ha−1, mean ± SE, n = 4 plots) of Quercus ilex, Phillyrea latifolia, Arbutus
unedo and the three species altogether in control plots and in drought plots during the period 1999–2005
Species
Quecus ilex
Phillyrea latifolia
Treatment
Leaves
Wood
Above-ground
Leaves
Wood
Above-ground
Control
Drought
41 ± 179
−15378 ± 15125
3510 ± 3368
1355 ± 2922
3555 ± 3350
−14023 ± 14462
68 ± 36
72 ± 37
1182 ± 637
1227 ± 628
1250 ± 673
1299 ± 665
Species
Forest
Arbutus unedo
Treatment
Leaves
Wood
Above-ground
Leaves
Wood
Above-ground
Control
Drought
153 ± 42a
29 ± 7b
2452 ± 1026a
311 ± 156b
2605 ± 1077a
580 ± 162b
260 ± 129
−15276 ± 1515
7230 ± 2440
3132 ± 2488
7490 ± 2560
−12144 ± 14069
Different letters indicate statistically significant differences between control and drought plots at t-test, P < 0·05 (a and b
between brackets when t-test, P < 0·1). Significant differences are highlighted in bold type. Forest refers to the three dominant
species together (they represents 98% of the total above-ground biomass).
Fig. 1. P and K concentrations (mean ± SE, n = 4), plot means in different biomass fractions of Quercus ilex in control and
drought plots in February 2005, after 6 years of experimental drought.
absolute biomass accumulation of leaves (75%), wood
(77%) and total above-ground growth (77%).
biomass concentrations
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
The P and K concentrations in 1999 were very similar
to those from 2005 for all species and biomass fractions (Table 2).
In Quercus ilex, drought increased P concentrations
in leaves (18·2%) and decreased P concentrations in
wood (30·9%) and roots (39·8%) (Fig. 1). Drought had
no effect on P concentrations in Phillyrea latifolia or
Arbutus unedo leaves, wood or litter. Drought had no
effects either on K concentrations in the different
fractions of the three studied species (Table 2).
p and k contents
P contents in wood and in total AB of Quercus ilex
decreased 15·9 kg P ha−1 (SE = 18·6, n = 4) (−21%, SE =
15·5) and 14·5 kg P ha−1 (SE = 17·5, n = 4) (−19·0%
SE = 14·2) after 6 years of drought; however, P contents
increased by 45·4 kg P ha−1 (SE = 17·6, n = 4) (33·7%,
SE = 6·5%) and 46·7 kg P ha−1 (SE = 18·0, n = 4) (33·1%,
SE = 6·3) in the control plots (Fig. 2). Drought had no
effects on the P contents in leaves and litter of Quercus
ilex (Fig. 2). This negative effect of drought on P biomass contents was due to both its negative effects on
biomass growth and on P concentrations.
Drought had no significant effects on P contents
in Phillyrea latifolia biomasses. Drought decreased P
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
Treatment
6·40 ± 0·37
6·17 ± 0·34
1·21 ± 0·05b
1·43 ± 0·10a
5·99 ± 0·50
5·63 ± 0·60
1·00 ± 0·08
1·17 ± 0·09
Leaves
Litter
3·40 ± 0·17
2·79 ± 0·39
1·06 ± 0·07
0·87 ± 0·05
2·98 ± 0·21
3·34 ± 0·19
1·01 ± 0·05(b)
1·18 ± 0·08(a)
Wood
3·89 ± 0·28
3·55 ± 0·41
1·28 ± 0·08
1·18 ± 0·12
4·02 ± 0·22
3·96 ± 0·31
1·81 ± 0·13a
1·25 ± 0·10b
3·30 ± 0·11
3·59 ± 0·25
1·28 ± 0·16a
0·77 ± 0·05b
Roots
9·32 ± 0·42
9·24 ± 0·38
1·26 ± 0·03
1·33 ± 0·03
8·14 ± 0·27
7·37 ± 0·52
1·22 ± 0·08
1·09 ± 0·07
Leaves
Phillyrea latifolia
2·75 ± 0·11
3·10 ± 0·20
1·08 ± 0·09
1·47 ± 0·18
2·73 ± 0·28
2·73 ± 0·21
1·28 ± 0·09
1·28 ± 0·10
Wood
Leaves
10·7 ± 0·8
12·3 ± 1·8
1·42 ± 0·16
1·42 ± 0·21
11·3 ± 0·5
10·7 ± 1·0
1·35 ± 0·04
1·34 ± 0·07
Litter
3·52 ± 0·27
3·64 ± 0·33
0·668 ± 0·135
0·506 ± 0·054
3·16 ± 0·19
3·75 ± 0·58
1·15 ± 0·13
1·00 ± 0·05
Arbutus unedo
3·42 ± 0·46
4·27 ± 0·75
1·27 ± 0·12
1·21 ± 0·11
3·50 ± 0·14
3·50 ± 0·15
1·26 ± 0·07
1·26 ± 0·07
Wood
3·76 ± 0·75
3·40 ± 0·67
0·793 ± 0·072
1·00 ± 0·11
3·86 ± 0·39
3·46 ± 0·40
1·03 ± 0·28
1·05 ± 0·07
Litter
Different letters indicate statistically significant differences between control and drought plots at t-test, P < 0·05 (a and b between brackets when t-test, P < 0·1). Significant differences are highlighted in bold type.
2005 (6 years treatment)
K
Control
Drought
P
Control
Drought
1999 (before treatment)
K
Control
Drought
P
Control
Drought
Element
Quercus ilex
Species
Table 2. Phosphorus (P) and potassium (K) concentrations (mg g−1, mean ± SE, n = 4 plots) in different biomass fractions of the three species studied in control and in drought plots
196
J. Sardans &
J. Peñuelas
Fig. 2. Increment (kg ha−1) in P and K content in leaf, wood
and total above-ground biomass in Quercus ilex and Arbutus
unedo plants in control and in drought plots. Different letters
indicate significant differences between control and drought
plots (t-test, P < 0·05).
Fig. 3. Increment (kg ha−1) in P and K contents in leaf, wood,
total above-ground biomass in the ecosystem (the sum of the
dominant tree species under study) in control and in drought
plots. Different letters indicate significant differences between
control and drought plots (t-test, P < 0·05).
contents in all of the analysed biomass fractions in
Arbutus unedo, although this effect was only marginally
significant (t-test, t = 3, d.f. = 6, P = 0·07) (Fig. 2). The
effect of the 6 years of drought at ecosystem level (taking
into account the three dominant tree species) was an
overall significant reduction in the total P contents in the
wood and total AB (leaves plus wood) in the ecosystem
(55 kg P ha−1) (t-test, t = 3·1, d.f. = 6, P = 0·02) (Fig. 3).
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accumulation
patterns
Table 3. Concentrations (mg g−1, mean ± SE, n = 4 plots)
of soil total phosphorus (P) and total potassium (K) in the
0 –15-cm deep soil and in the 15 –30-cm deep soil
Fraction
Treatment
0 –15 cm
depth
15 –30 cm
soil depth
Soil total P
C
D
DD
C
D
DD
0·598 ± 0·031
0·605 ± 0·028
0·543 ± 0·028
15·5 ± 0·3b
15·0 ± 0·3b
17·0 ± 0·3a
0·546 ± 0·022
0·539 ± 0·027
0·539 ± 0·014
15·3 ± 0·3b
16·4 + 0·3a
16·7 ± 0·5a
Soil total K
Different letters indicate statistically significant differences
(anova, Bonferroni post-hoc test, P < 0·05). Significant
differences are highlighted in bold type. C = Soil of control
plots; D = soil of drought plots situated between plastic strips
(runoff exclusion); DD = soil of drought plots situated below
plastic strips (runoff plus rainfall exclusion).
Drought had no significant effects on the K content
in any species or fractions analysed (Figs 2 and 3),
although trends towards an increase in the K aboveground content in Quercus ilex and Phillyrea latifolia
and towards a reduction in Arbutus unedo, were observed
as a response to drought (Fig. 2).
The amounts of P and K loss in litterfall (kg ha−1)
for these three species together during 2004 were greater
in drought plots 1·97 (SE = 0·20, n = 4) and 6·05 (SE =
0·20, n = 4), respectively, than in control plots 1·59
(SE = 0·20, n = 4) and 5·05 (SE = 1·45, n = 4), respectively,
but these differences were not statistically significant.
soil concentrations
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
Drought had no effects on the total P soil concentrations, although it did increase the K in the soil both at
depths of 0 –15 cm (10%) and at 15–30 cm (8·6%)
(Table 3).
Drought conditions increased the total soil soluble
P (Olsen-P) and soil organic soluble P (Olsen-Porganic)
(Fig. 4), but not soil inorganic soluble P (Olsen-Pinorganic)
in the January 2005 sample. In addition, a decrease in
the ratio of inorganic : organic soil soluble P fractions
(Olsen-Pi : Po) by 50% in the first 15 cm of the soil layer
(Fig. 4) and by 183% between 15 and 30 cm in the soils,
under transparent plastic strips. Drought produced
similar effects on P soil fractions in the soil sample
collected in April 2005.
Drought decreased soil available K (NaNO3 extractable K) both at 0 –15 cm (Fig. 5) and at 15–30 cm
depths (20% and 19%, respectively) in the soil sampled
in January 2005; drought thus decreased the ratio
between available K : total soil K (NaNO3 extractable
K and total K) at 0 –15 cm (20%) (Fig. 5) and 15–
30 cm (14%) depths. Similarly, drought decreased soil
available K (NaNO3 extractable K) both at 0–15 cm
depths and at 15 –30 cm depths (37% and 44%, respectively) in the soil sampled in April.
Fig. 4. Concentrations (mg g−1) of different fractions of P in
soil (0 –15 cm depth). Different letters indicate statistically
significant differences (anova, P < 0·05). C = Soil of control
plots. D = Soil of drought plots between plastic strips (runoff
exclusion). DD = Soil of drought plots below plastic strips
(runoff plus rainfall exclusion). Pi = inorganic phosphorus.
Po = organic phosphorus.
Discussion
phosphorus in above-ground biomass
and soil
Total P content in AB decreased by approximately
one-third after 6 years of moderate drought. Although
drought increased the P concentration in leaves, a
drought-induced reduction in LB means that there was
no increase in the leaf P contents at ecosystem level. In
fact, after 6 years of drought, there was a decrease in
above-ground P contents in Quercus ilex due to both
the decrease in P wood concentrations and the decrease
in wood biomass (Ogaya & Peñuelas 2007). The
observed tendency of drought to decrease P contents
in wood and total AB in Arbutus unedo was mainly due
to the negative effect of drought on stem growth.
Drought increased the soil soluble Porganic, but not
the soil soluble Pinorganic that is the directly available P
source for plants, thereby decreasing the soil soluble
Pinorganic : Porganic ratio. Drought slowed down the release
of soluble ortophosphate from organic to inorganic
forms, leading thus to an accumulation of soluble
a change in humus quality as a result of decreased
microbial activity, which can reduce the soil K-soluble
retention capacity. Drought frequently increases sclerophylly (Bussotti et al. 2002; Bacelar et al. 2004) and
sclerophylly can often decrease the nutritional quality
of plant tissues owing to the higher concentrations
of structural compounds such as lignin (Pérez 1994;
Feller et al. 1999). A significant presence of structural
compounds hinders the mineralization processes.
However, in the present study, the negative effect of
drought on mineralization rates could not be imputed
to an increase in LMA (Leaf Mass Area), which
remained unchanged (Ogaya & Peñuelas 2006).
198
J. Sardans &
J. Peñuelas
differences between phosphorus and
potassium responses
Fig. 5. Concentrations of NaNO3 extractable soil K (mg g−1)
and soil ratio NaNO3 extractable K : Total K soil (0 –15 cm
depth). Different letters indicate statistically significant
differences (anova, P < 0·05). C = Soil of control plots. D = Soil
of drought plots between plastic strips (runoff exclusion).
DD = Soil of drought plots below plastic strips (runoff plus
rainfall exclusion).
organic forms in the soil and consequently an increase
in total soluble P. The decrease in the soil soluble
Pinorganic : soil soluble Porganic ratio produced by drought
is related to the decrease in soil enzyme activity
induced in these soils by drought (Sardans & Peñuelas
2005) and agrees with previous studies in the same
forest (Sardans & Peñuelas 2004). The reduction in
mineralization rates as a result of drought has also been
observed in other Mediterranean ecosystems (Gorissen
et al. 2004). All these results indicate that drought leads
to diminished plant P uptake of nutrients and greater
recalcitrance in the soil.
potassium in above-ground biomass
and soil
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
The 6 years of drought reduced the soil K-extractable
content but increased the soil total K content, indicating
a slowdown in meteorization and /or mineralization
rates. Several studies have shown that drought reduces
soil K release capacity (Ruan et al. 1997; Oliveira,
Rosolem & Trigueiro 2004; Kaya, Higgs & Kirnak 2005)
and can thus increase K accumulation in the soil. In
this case, the most likely explanation for K accumulation in the soil is the decrease in meteorization rates
and to a lesser extent the decrease in soil enzyme activity (Sardans & Peñuelas 2005), which generates a
reduction in the soluble forms in the soil and an accumulation of unavailable forms. Another possible cause
of the reduction in the concentrations of soluble K
forms in the soil and the increase in the total soil K, is
P foliar concentrations were changed by the drought
treatment but K foliar concentrations were not. The
increases in P concentrations as a response to drought
conditions have been widely reported (Utrillas, Alegre
& Simon 1995; Díaz & Roldan 2000; Samarah, Mullen
& Cianzio 2004) and have been related variously to an
increase in water-use efficiency (Díaz & Roldan 2000;
Graciano, Guiamét & Goya 2005), to a drought-resistance mechanism (Egilla, Davies & Drew; Egilla et al.
2005; Samarah et al. 2004) and/or to a decrease in
the dilution effect (Sabaté & Gracia 1994; Peñuelas &
Estiarte 1998). The increase in P leaf concentrations
and the decrease in root and stem concentrations
suggest a mobilization of P from wood towards leaves
in order to improve the water-use efficiency.
The 6 years of drought generated different responses
of P and K also at the ecosystem level. Whereas drought
decreased P contents in AB and increased total soil
soluble P without affecting soil soluble inorganic P,
drought did not change K contents in AB, reduced
soil-soluble K in the soil, and increased total soil K.
Two differences in the geochemical traits of these
two nutrients account for the different results obtained.
First, K is more mobile than P and therefore P absorption is more dependent on the capacity of roots to
explore new soil volumes (given the low mobility of P
in soil when compared with K). Secondly, soil K is in
mineral form and only a minimal proportion of K resides
in organic matter and litter, whereas in P the proportion of P in organic forms and litter with respect to
total P soil is greater. Drought decreases soil enzyme
activity (Sardans & Peñuelas 2005), thereby decreasing
soil soluble inorganic P and the capacity of soil to supply
P to plants. This effect together with the decrease in
growth in AB accounted for the reduction of P accumulation in AB in the plants subject to drought conditions. K soil contents were greater in drought plots
because K mostly resides in silicates and both solubility
and meteorization is reduced if soil moisture decreases,
which in turn will lead to an increase in total K and
decrease in soluble K in soils of drought plots. K contents
in AB did not change in drought soils probably because
199
Drought changes
P and K
accumulation
patterns
the decrease in soil moisture was insufficient to generate
changes in K plant capture. In this context, the rewetting
effect assures significant K capture, even in drought plots.
differences in plant resp onses
Drought changed P concentrations and accumulation
patterns in Quercus ilex and Arbutus unedo more than
in Phillyrea latifolia. This different response may lead
to changes in competitive ability and eventually changes
in the species composition of the plant community in
favour of shrub species. This different response in
nutrient status as a result of drought coincides partially
with these species’ different growth responses (Ogaya
et al. 2003; Ogaya & Peñuelas 2007), mortality (Ogaya
et al. 2003; Ogaya & Peñuelas 2007) and reproductive
effort and seed recruitment (Lloret, Peñuelas & Ogaya
2004; Ogaya & Peñuelas 2004). The effect of drought
on AB accumulation in the period 1999–2005 was also
different between species: in Arbutus unedo the AB
accumulation fell significantly, in Quercus ilex there
was a tendency for AB accumulation to drop, and in
Phillyrea latifolia there were no effects at all on AB
accumulation (Ogaya & Peñuelas 2007).
possible implications: nutrient losses
and stoichiometric changes
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 191–201
As torrential rainfall is typical of the Mediterranean
region (Ramos & Porta 1994) and it is predicted to
become more extreme and frequent in the near future
(Houghton et al. 2001; Peñuelas et al. 2005), and as P
and K losses during a single sudden rainstorm may
be very high (Ramos & Martínez-Casanovas 2004),
greater losses of P and K are thus likely to occur over
the coming decades in these Mediterranean ecosystems.
The rewetting effect during rainfall should increase the
amounts of mobilized P and K, thereby increasing the
possibility of P and K ecosystem losses during torrential rainfall.
Another possible implication of lower P and/or K
content and availability in soil may be an enhancement
of the usual increase in the below-ground : AB ratio
observed in Mediterranean forests (Keith, Raison &
Jacobsen 1997). As drought can also directly increase
the below-ground : AB ratio (Noordwijk et al. 1988;
Jose, Merritt & Ramsey 2003; Chiatante, Di Iorio &
Scippa 2005), a reduction in AB more than in belowground biomass can be expected under future arid
conditions in those ecosystems.
The differing effects of drought on the accumulation
of P and K in the biomass changes the stoichiometry
between these two nutrients in this ecosystem and affects
the proportional availability of these two nutrients to
trophic chains. Changes in nutrient concentration ratios
in plants, affect trophic chains and are likely to produce
shifts in the composition of herbivore communities
and in the specific selection of plants by herbivores as
food sources (Makino et al. 2003; Ngai & Jefferies 2004;
Diehl, Berger & Wohrl 2005). If drought increases
as fast as climate models predict, a period with rapid
changes in nutrient ratios will favour species with more
flexible body compositions. This could negatively affect
the resistance of the ecosystem to drought in Mediterranean ecosystems, as species of some taxonomic groups
such as invertebrates (Drosophila sp., Daphnia sp.) with
flexible body compositions have low physiological
functioning efficiencies (Jaenike & Markow 2003) and
their capacity to respond to water availability reduction may be hampered. Furthermore, although it has
been suggested that terrestrial plants have limited
capacity of changing their body composition (Zhang,
Bai & Han 2004), some recent experiments have shown
that Mediterranean plants change their nutrient composition under different environmental conditions but
in different proportions depending on the species, e.g.
Pinus halepensis and Quercus ilex saplings and on the
elements (Sardans, Rodà & Peñuelas 2006c).
Acknowledgements
This research was supported by the Spanish Government REN2003-04871/GLO, CGL2004-01402/BOS
and CGL2006-04025/BOS grants, the EC Integrated
FP6 ALARM (GOCE-CT-2003–506675) Project, a
Fundación BBVA 2004 grant and the Catalan government SGR2005-00312 grant. This experiment complied
in all aspects with the laws of the Spanish State and the
European Union.
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Received 25 October 2006;accepted 14 December 2006
Editor: James Cresswell