AC TA O E C O L O G I CA
29
(2006) 221–232
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/actoec
Original article
The effects of nutrient availability and removal
of competing vegetation on resprouter capacity
and nutrient accumulation in the shrub Erica multiflora
J. Sardans a,*, J. Peñuelas a, F. Rodà b
a
Ecophysiology Unit CSIC-CEAB-CREAF. CREAF (Center for Ecological Research and Forestry Applications), Autonomous University
of Barcelona, E- 08193 Bellaterra, Spain
b
Department of Animal and Plant Biology and Ecology, CREAF (Center for Ecological Research and Forestry Applications) and Unit
of Ecology, Autonomous University of Barcelona, E-08193 Bellaterra, Spain
A R T I C L E
I N F O
Article history:
Received 29 March 2005
Accepted 25 October 2005
Available online 18 January 2006
Keywords:
Calcareous soil, Competition
Nitrogen
Mediterranean shrubland
Phosphorus
Post-fire
Resprout branching
A B S T R A C T
Nutrient availability is increasing in the Mediterranean Basin due to the great number and
intensity of fires and higher levels of anthropomorphic pollution. In the experiment described in this paper, we aimed to determine the effects of N and P availability and of the
removal of competing vegetation on resprouter capacity, biomass, and nutrient accumulation in Erica multiflora. Plants of the resprouter species E. multiflora were clipped to 0% of
aerial biomass in a post-fire Mediterranean shrubland and fertilisation experiments and
removal of competing vegetation were established in a factorial design. The resprouting
of clipped plants was monitored during the first year after clipping and at the end of the
year, all plant resprout populations were harvested and their resprout structure, biomass
and N and P content measured. N fertilisation had no significant effect on leaf biomass
either at plant level or on the total aerial biomass per stump unit area; however N concentration in resprout biomass did increased. P fertilisation slightly increased resprouting vigour and had a significant effect on P content of the leaf biomass. The removal of competing vegetation increased the ratio between leaf biomass and stem biomass, the lateral
expansion of resprout, the hierarchy of resprouts branching, and the P content of stems,
above all when P fertilisation was applied. These results show that as a response to decreased competition E. multiflora has the capacity to modify the relative proportions of
the nutrients in the aerial biomass. All these characteristics allow E. multiflora to persist
in increasingly disturbed Mediterranean ecosystems and contribute to the retention of
nutrients in the ecosystem during early resprouting phases.
© 2006 Elsevier SAS. All rights reserved.
1.
Introduction
In Mediterranean ecosystems, the high cost of biomass production together with the considerable levels of natural damage (recurrent fires, severe dry periods, and herbivore pres-
*
Corresponding author. Tel.: +93 581 13 12; fax: +93 581 41 51.
E-mail address: [email protected] (J. Sardans).
sure) are proposed as general explanations for resprouting
capacity (Mooney and Dunn, 1970; Lloret et al., 1999). This reproductive strategy enables plants to immediately recover
lost ground and has even been considered in ecological theory auto-succession (Hanes. 1971).
In general, Mediterranean ecosystems are considered to
be poor in nutrients (Mooney and Dunn, 1970; Ellis and Kummerow, 1989). On the other hand, there is evidence of the role
played by nutrients in limiting resprouting capacity (Prevost,
1146-609X/$ - see front matter © 2006 Elsevier SAS. All rights reserved.
doi:10.1016/j.actao.2005.10.006
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1994; Cruz and Moreno, 2001). Resprouting capacity should
be especially important in nutrient-poor environments and
in environments such as Mediterranean ecosystems where
there is a great risk of post-fire nutrient losses caused by torrential rainfalls.
Some experiments have demonstrated that resprouting
vigour is strongly reduced by the presence of competing vegetation. Resprouting should be stronger when a perturbation has destroyed not only the biomass of a single plant
but also that of its neighbours (Vilà and Terradas, 1995a,
1998; Vilà et al., 1998). Less is known about the interaction
between nutrient availability and the presence of competing
vegetation on patterns of resprouting intensity, on the nutrient capture during resprouting and on the structure of
sprouts population of each plant.
In some studies, competition has been considered to have
a more relevant role in nutrient-rich than in nutrient-poor
environments (Grime, 1977; Reader, 1990); in others, however,
competition has been reported to be equally important in
rich and poor environments (Tilman, 1982; Wilson and Tilman, 1993). The idea that the intensity of competition depends on resource availability in ecosystems remains controversial (Welden and Slauson, 1988; Peltzen and Kochy, 2001).
Most experiments carried out on the interaction between
competition and nutrient supply levels have been conducted
by removal of competing vegetation. These experiments
have been conducted mostly in grassland communities (see
Tilman, 1990) and less often in Mediterranean shrublands
(Vilà and Terradas, 1995a). Furthermore, two different structural levels can be distinguished in a context of plant competition. The first level is represented by genetic individuals in
the population that are the result of sexual reproduction; the
second level is found within individual plants and is the result of their modulated growth pattern. At this second level,
competition exists between different modules within the
same plant (Berstson and Weiner, 1991).
During the last century, the temperature in the Mediterranean Basin showed an overall trend towards warming (Piñol
et al., 1998; Peñuelas et al., 2002; Peñuelas and Boada, 2003)
and precipitation levels are currently experiencing a longterm downward trend in some Mediterranean areas (Kutiel
et al., 1996; Esteban-Parra et al., 1998). This change in climate
is occurring simultaneously with changes in nutrient availability in many areas of the Mediterranean Basin. Fire frequency has increased in the eastern part of the Iberian Peninsula in recent decades (Pausas, 2004). Frequent fires may
result in cumulative nutrient loss through volatilisation,
smoke particles, windblown ashes, soil leaching, and erosion, thereby magnifying the possible limiting role of nutrients. Fire can increase N and P availability in the initial period after fire (Carreira et al., 1996; Gimeno-García et al., 2000).
However, this sudden increase in P availability only last for a
short time due to the fact that such increases principally occur in soluble P in inorganic soil (Kutiel and Kutiel, 1989; Thomas et al., 1999). Moreover, P losses caused by volatilisation
(Soto et al., 1997) or rainfall erosion (Thomas et al., 1999) can
often be higher after fire. The capacity of quick absorption of
nutrients after a fire event has been suggested as one of the
benefits of a resprouting strategy (Specht, 1973; Romanya et
al., 2001) and, in this way, the liberated nutrients can easily
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(2006) 221–232
be retained by the resprouting species following a disturbance. Another driver of change in nutrient availability is
the alteration of global biogeochemical cycles by human activities. The global N cycle has now reached the point in
which more N is fixed annually by human-driven processes
(fertilisers, combustion of fossil fuels, and waste from stockraising) than by natural processes (Vitousek et al., 1997). Nitrogen inputs and N and P foliar concentrations seem to have
increased in some Mediterranean species in the last few decades (Peñuelas and Filella, 2001).
The capacity to capture nutrients may become a vital part
of the ecological strategies of Mediterranean plants in context of a global change, in which a decrease of water availability, more erratic and torrential rainfalls, greater erosion,
and increased fires and nutrient deposition may lead to steeper gradients in nutrient supply and thus affect the regenerative capacity of the Mediterranean sclerophyllous ecosystems. This new environmental scenario may challenge the
capacity of sprouting strategies and their role in the maintenance of the structure of present-day Mediterranean ecosystems. The capacity to capture nutrients under different levels
of competition and nutrient availability may be the key for
Mediterranean resprouters to maintain their current areas
of distribution and retain nutrients in the ecosystem in the
near future.
Erica multiflora is a common evergreen shrub that typically
occurs in coastal shrublands on calcareous soils in the western Mediterranean Basin (Orshan, 1989). Its resprout vigour
has been studied in light of a number of different disturbances (Lloret and López-Soria, 1993); water stress (Vilà and
Terradas, 1998; Llorens et al., 2003), warming (Llorens et al.,
2004), competing vegetation (Vilà, 1997) and herbivores (Vilà
and Lloret, 1996; Vilà et al., 1998). The current coincidence
between climate change and increase in nutrient supplies
warrants an investigation of the capacity of dominant Mediterranean shrubs to change their sprout structure and to
capture and retain nutrients in their biomass in response to
nutrient pulses originating from forest fires or pollution.
In a post-fire shrubland with a history and a structure typical of widespread zones of the Mediterranean Basin, we
conducted a factorial design experiment involving nutrient
fertilisation and the removal of competing vegetation as
way of studying to study the effects of disturbance on
E. multiflora, a typical Mediterranean resprouting shrub species. Our aims were to investigate the effects of a sudden increase in N and P supplies and different densities of competing vegetation on (i) resprouting vigour and structure
(biomass, number, size, and branching distribution of resprouts at genet level), and (ii) the nutrient content of the resprouts.
2.
Materials and methods
2.1.
Experimental site
The experiment was conducted in a naturally regenerated
post-fire shrubland that was burnt three times in the period
1965–1985. The last fire occurred in summer 1985, 5 years before the experiment started. The study site was located on a
ACTA OECOLOGICA
level hill top (slope 0–5%) in the pre-coastal mountain range
of central Catalonia at 300 m above sea level (41°37′ N, 1°50′
E). In this area, a Lithic haploxeroll soil associated with Lithic
xerorthens soils exist over Eocenic calcareous-loam rocks of
sedimentary origin. The soil has a high pH (8.3 ± 0.2) and
high proportions of carbonates (55.9 ± 1.2%) and active lime
(12.2 ± 0.5%) (Sardans, 1997). The soil extractable NO3– and
NH4+ were 9.59 ± 0.77 and 0.73 ± 0.07 mg kg–1 soil, respectively (Sardans, 1997). The bicarbonate-extractable P in soil
was low (4.05 ± 0.3 mg P kg–1 soil). The climate is Mediterranean with a moderate continental component. The annual
average temperature is 14 °C, with the average minimum
temperature of the coldest month being –1.9 °C and the average maximum temperature of the hottest month being 31.
8 °C. Mean annual rainfall is 517 mm (period 1985–1996) and
the summer drought period comprises 3 months from June
to September. The vegetation type is a post-fire Mediterranean shrubland (Erico Thymalaeetum tinctoreae) with young
saplings of Aleppo pine (Pinus halepensis) and small resprouts
of interior holm oak (Quercus ilex subsp. rotundifolia). The total
plant cover when the experiment started (1990) was 77.5
± 3.7%. The most abundant species were P. halepensis (29.3
± 6.1%), Rosmarinus officinalis (15.7 ± 3.7%), Brachypodium retusum (10.1 ± 4.1%), Thymus vulgaris (4.5 ± 1.98%), and
E. multiflora (4.1 ± 1.6%).
2.2.
Experimental design
We established two different experimental designs in order
to study separately the effects of N and P fertilisation. Each
of the experimental designs had two factors: N or P fertilisation and the removal of competing vegetation, and consisted
of four treatments—C (Control) and R (removal of competing
vegetation treatment without fertilisation), N and NR (fertilisation with equivalent doses of 500 kg N ha–1 with and without competing vegetation), or P and PR (fertilisation with
equivalent doses of 250 kg P ha–1 with and without competing vegetation). These designs enabled us to investigate the
possible effects of N and P supplies, the competitive pressure
within resprouting, and the interactions between N and P
and competition. We assigned 21 genets randomly to each
treatment. Due to the heterogeneity of the plot area, the design was completely random and a block design was discarded.
Aerial biomass was completely removed from all the
plants to simulate a strong perturbation and to allow subsequent resprouting while the subterranean biomass was not
altered. The treatments were applied to individual plants.
Fertilisation consisted of hand application of doses equivalent to 250 kg P ha–1 of calcium phosphate and 500 kg N
ha–1 of ammonium nitrate. These doses were chosen as they
have been employed in several previous experiments using
nutrient manipulation and are considered to be of intermediate intensity (Mayor and Rodà, 1994). The fertilisation treatments were conducted in July (the month with the highest
frequency of fires). In both cases the fertiliser was dispersed
homogeneously in a 1 m2 circle around the target plants. The
removal of competing vegetation consisted of the complete
removal of all competing aerial biomass in a 1 m2 circle
around the target stump. This method has been shown to re-
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223
duce competition in previous field experiments on shrublands and grasslands and is regarded to be an efficient way
of detecting the presence of competition (Aarseen and Epp,
1990). The removal of competing vegetation was continued
throughout the experiment in order to completely suppress
this pressure. Target plants were kept at least 4 m apart in
order to avoid treatment interferences. The average distance
between target plants in the field was 6.3 ± 1 (S.E.) m.
2.3.
Measurements and sampling of biomass
The basal area of stumps was measured at the beginning of
the experiment after sprouts had been removed. No differences in the mean size of the individuals assigned to each
treatment were detected, thereby assuring the homogeneity
and equal distribution of plant sizes across the different
treatments.
The number of resprouts from every stump (the resprout
number) was measured every two months in order to monitor the evolution of sprouting. One year after the beginning
of experiment, resprouts of all the experimental plants were
harvested. The following measurements were taken: (1) total
number of resprouts of each plant; (2) basal diameter, height
and number of lateral branches of each resprout; (3) total biomass, leaf biomass and stem biomass of each plant; (4) N
and P concentration in the leaves and stems of the resprouts
and (5) N and P content of the total biomass and stem and
leaf fractions.
2.4.
Chemical analyses
Leaves and stems were dried in an oven at 70 °C for 48 hours
until a constant weight was reached. Seven replicates of each
biomass fraction per treatment were analysed. Nitrogen concentrations were analysed by the Kjeldhal method in a KJELTEC 1030 autoanalyser (RECATOR, Höganäs, Sweden) after
acid digestion (with H2SO4 + Devarda catalyst) conducted in
a Tecator digester (TECATOR, Höganäs, Sweden). Phosphorus
concentration was analysed by ICP-AES (Atomic Emission
Spectroscopy with Inductively Coupled Plasma) (in a spectrophotometer JOBIN YBON JI 38, JOBIN, France) after biacid digestion (HNO3/HClO4, 2:1) in a microwave oven (SAMSUNG,
Seoul, South Korea).
2.5.
Statistical analyses
The normality distributions of all the variables analysed
were tested by the Kolmogorov–Smirnov test (Statistica 6.0,
StaSoft Inc., Tulsa, OK, USA). The effects of treatments on
leaf, stem and total aerial biomass, on number of resprouts
per plant, and on N and P concentration and contents at the
end of the experiment were analysed by factorial ANCOVA
(with the plant stump area as cofactor). When the cofactor
was not significant, a factorial ANOVA was used (Staview
5.0.1, SAS Institute Inc., Berkeley, CA, USA). When significant
differences were detected, a mean contrast between treatments was conducted by the Duncan new multiple range
test. When the plant stump area explained a significant part
of the variance, the significance of this effect was analysed
by a regression analysis. For analyses of the experimental
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factors on the ratio between leaf and stem biomass growth,
an ANCOVA with stem biomass growth as a covariable was
used, given the possible dependence of the ratio values of
the denominator (Jackson et al., 1990; Liermann et al., 2004).
To investigate the competition within plant modules, resprout size and branching distribution in each genet was statistically analysed to determine the effect of treatment on
the intra-plant population traits used as an estimation of
the structure of the resprout population of each plant. The
statistical tests used for this purpose were: the coefficient of
variation (CV), the skewness coefficient (g) and the Gini hierarchy coefficient (G). These coefficients were calculated as in
Bendel et al. (1989) and have been widely used to analyse the
structure of biological populations. CV assesses the deviation
value with respect to the mean value while skewness assesses the degree of asymmetry of the distribution around
the mean as the difference in the grouping at the two extremes of the distribution. While the skewness coefficient
assesses the proportion of the individuals of different sizes,
the Gini coefficient assesses the hierarchy of population distribution and has an intuitive significance for ecological studies (Weiner and Solbrig, 1984). For more information on
these coefficients, see Sen (1973). The values of the three
coefficients in the population distribution of each plant
sprout were statistically analysed by ANOVAs in order to detect experimental treatment effects. In all the analyses, the
significant level was established below P = 0.05.
The intensity (IN) and the importance (IM) of the effects of
competition (Welden and Slauson, 1988) on the sprouting
biomass and on N and P content were also analysed by the
ANOVA results. The following equations were used to calculate these variables:
IN = (NC – C)/C IM = (SC/ST) 100
NC = Variable mean value of the plants with removal of
competing vegetation.
C = Variable mean value of the plants without removal of
competing vegetation.
SC = Variance explained by removal of competing vegetation.
ST = Total variance.
To estimate the degree of significance of the values obtained for the importance and the intensity of competition,
we conducted an ANOVA analysis within the variable of C
with respect to R, of N with respect to NR, and of P with respect to PR.
3.
Results
3.1.
Resprouting vigour
Removal of competing vegetation had no effect on either total biomass or number of resprouts on each plant although
there was an increase in the ratio between leaf biomass and
stem biomass in plants when either P (P = 0.006) and N fertiliser was applied (P = 0.046) (Tables 1 and 2). Stem biomass
had a significant effect (P = 0.028) on the ratio between leaf
and stem biomass in the design of N fertilisation × Removal
of competing vegetation but not in the design P fertilisation ×
Removal of competing vegetation (Table 1).
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No general effects of N fertilisation on resprouting vigour
were observed other than a significant decrease in the ratio
between leaf and stem biomass and in mean height of the
sprouts of each plant (Table 1). N fertilisation also decreased
the number of sprouts in the plants at the end of the first
year after clipping (F = 2.1, P = 0.11) although not significantly.
A negative interaction between N fertilisation and the removal of competing vegetation was detected in leaf, stem
and total biomass growth (Table 1). Plant growth under N fertilisation and the removal of competing vegetation was lower
than growth under N fertilisation alone, under the removal
of competing vegetation alone, and in the controls. The
stump area had a positive effect on biomass leaf and stem
biomass and a negative effect on the growth relative to
stump area (Table 1).
The total biomass of resprouts of the plants fertilised with
P was higher (8.12 ± 1.39 g) than in the unfertilised plants
(5.63 ± 0.77 g), but this difference was not significant (F = 2.8,
P = 0.12). P fertilisation had no effect on the other variables
affecting resprouting vigour (Tables 1 and 2). No interactions
were observed between the removal of competing vegetation
and P fertilisation.
No trends were found in the importance and intensity of
competition due to N or P fertilisation other than in the ratio
between foliar and stem biomass (comparison between C
and R: 0.05% importance in control plots versus 12.6% in Pfertilised plants, P = 0.018 in the ANCOVA). Thus, the percentage of the total variability accounted for by the removal of
competing vegetation increased when P fertilisation was applied (Table 3). The effects of competition on the biomass of
the plant resprout population decreased when P fertilisation
was applied, but tended to increase when N fertilisation was
applied (Table 3). A decrease in biomass of the resprout plant
was observed when N fertilisation was applied without the
removal of competing vegetation.
Neither fertilisation nor the removal of competing vegetation had any significant effect on branching number of the
plant sprouts (Table 2). No interactions were observed between N fertilisation and removal of competing vegetation
or between P fertilisation and the removal of competing vegetation on number of sprouts or on the branching number
of plant sprouts (Table 2).
3.2.
Population structure of the resprouts of each genet
The mean number of resprouts per plant was 35.4 (± 3.2 S.E.).
Removal of competing vegetation significantly increased the
three coefficients CV, g and G for the number of branches
when P but not N was applied (Table 4). The removal of competing vegetation did not significantly change any of the
three coefficients CV, g and G for the distribution of height
and basal diameter in the resprout population of each plant
(Table 4). These results show an increase in dispersion
around the mean together with a higher hierarchy of the distribution of the sprout branches in an individual plant sprout
population. No significant differences in these coefficients
were detected as a response to N or P fertilisation (Table 4).
There was a positive correlation between the basal diameter
of the resprout and the number of the ramifications on these
resprouts under all treatments (r = 0.8, P = 0.001, n = 21). No
ACTA OECOLOGICA
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Table 1 – Leaf, stem and total aerial biomass of the plants (g; mean ± S.E.), the mean height of the resprouts of each plant
(mm; mean ± S.E.), leaf, stem and total aerial biomass of the plants per stump area of the plant, and ratio between leaf
biomass and stem biomass of all plant sprouts in the different experimental factors in the factorial designs experiments.
All the variables are represented by the values reached after a year of clipping and fertilisation. Significant differences
(P < 0.05) between treatments are highlighted in bold type. Different letters in brackets indicate significantly different
values. The significant levels (P) of the two factors and their interaction in the factorial ANOVA design for each dependent
variable are given in the final three columns. (Nf = N fertilisation, R = Removal of competing vegetation, Pf = P fertilisation).
If an ANCOVA was used, it is indicated by the P value of the cofactor (stump area or stem biomass)
Design: N fertilisation · Removal of competing vegetation
Variable
P stump C
R
area
Leaf biomass
Stem biomass
Total biomass
Mean height of the
resprouts of each
Leaf biomass/
stump area
Stem biomass/
stump area
Total biomass/
stump area
N
NR
P for R
P for Nf P interaction
0.012
0.014
3.22 ± 0.55 (a)
1.88 ± 0.33 (a)
5.15 ± 0.86 (a)
135 ± 11 (a)
3.96 ± 0.81 (a)
2.15 ± 0.49 (a)
6.10 ± 1.30 (a)
134 ± 11 (a)
2.44 ± 0.59 (a)
1.55 ± 0.40 (a)
4.02 ± 1.00 (a)
90 ± 9 (b)
3.49 ± 0.85 (a)
1.97 ± 0.50 (a)
5.41 ± 1.34 (a)
111 ± 11 (a)
0.691
0.759
0.711
0.902
0.100
0.206
0.142
0.043
0.027
0.049
0.032
0.749
0.0007
0.071 ± 0.011 (a)
0.110 ± 0.026 (a)
0.059 ± 0.022 (a)
0.053 ± 0.011 (a)
0.716
0.081
0.006
0.0023
0.040 ± 0.006 (a)
0.059 ± 0.015 (a)
0.037 ± 0.016 (a)
0.031 ± 0.007 (a)
0.948
0.292
0.015
0.012
0.111 ± 0.017 (a)
0.170 ± 0.041 (a)
0.096 ± 0.039 (a)
0.084 ± 0.170 (a)
0.714
0.141
0.032
1.11 ± 0.19 (b)
1.43 ± 0.20 (b)
0.046
0.001
0.962
P
PR
P for R
P for Pf
P interaction
5.28 ± 1.32 (a)
3.54 ± 1.07 (a)
8.81 ± 2.37 (a)
150 ± 9 (a)
4.86 ± 1.10 (a)
2.74 ± 0.68 (a)
7.60 ± 1.78 (a)
150 ± 11 (a)
0.671
0.826
0.866
0.923
0.502
0.944
0.678
0.222
0.392
0.221
0.310
0.935
0.094 ± 0.025 (a)
0.106 ± 0.017 (a)
0.181
0.245
0.144
0.065 ± 0.021 (a)
0.058 ± 0.010 (a)
0.589
0.433
0.178
0.158 ± 0.045 (a)
0.164 ± 0.026 (a)
0.312
0.354
0.118
1.55 ± 0.14 (a)
1.98 ± 0.12 (b)
0.006
0.934
0.793
P stem
biomass
Leaf biomass/Stem 0.028
1.63 ± 0.17 (a)
1.93 ± 0.12 (a)
biomass
Design: P fertilisation · Removal of competing vegetation
Variable
P stump
C
R
area
Leaf biomass
0.003
3.22 ± 0.55 (a)
3.96 ± 0.81 (a)
Stem biomass
0.047
1.88 ± 0.33 (a)
2.15 ± 0.49 (a)
Total biomass
0.018
5.15 ± 0.86 (a)
6.10 ± 1.30 (a)
135 ± 11 (a)
134 ± 11 (a)
Mean height of the
resprouts of each
plant
Leaf biomass/
0.028
0.071 ± 0.011 (a) 0.110 ± 0.026 (a)
stump area
Stem biomass/
0.0001
0.040 ± 0.006 (a) 0.059 ± 0.015 (a)
stump area
Total biomass/
0.045
0.111 ± 0.017 (a) 0.170 ± 0.041 (a)
stump area
P stem
biomass
Leaf biomass/Stem
1.63 ± 0.17 (a)
1.93 ± 0.12 (b)
biomass
C = control, without N fertilisation and without removal of competing vegetation; N = with N fertilisation and without removal of competing
vegetation; R = without N fertilisation and with removal of competing vegetation; NR = with N fertilisation and removal of competitive vegetation; P = with P fertilisation and without removal of competing vegetation; PR = with P fertilisation and with removal of competing vegetation.
effect of stump basal area on sprout population structure or
interactions between experimental factors was observed
(Table 4).
3.3.
N and P concentrations and contents
The removal of competing vegetation significantly increased
(F = 6, P = 0.017) the P concentration in stems, above all when
P fertiliser was applied. A significant interaction was observed between P fertilisation and removal of competing vegetation (F = 32, P < 0.0001) in the sense that P fertilisation
had a greater positive effect on P concentration principally
when neighbours were removed (Fig. 1 and Table 5). The removal of competing vegetation had no other significant effects on nutrient concentration (Fig. 1). When P fertiliser
was applied, the importance and intensity of competition increased the concentration of P in leaf and stem (Table 5).
These effects were not observed as a response to N fertilisa-
tion (Table 5). No interactions between treatments were observed in biomass concentration.
The addition of N fertiliser significantly increased the
concentration of N in leaves (F = 4.7, P = 0.036) and stems
(F = 6.2, P = 0.013). N fertilisation had no significant effect on
P concentrations (Fig. 1). The addition of N fertiliser and the
removal of competing vegetation tended to decrease N and P
contents in the plant leaves and stems, although these effects were not statistically significant (Fig. 2).
Addition of P fertiliser significantly increased (42%) concentration P in leaves (F = 9.7, P = 0.0003), but not in stems
(F = 1.15, P = 0.381) (Fig. 1). The highest concentrations of P
in leaves were found when P fertilisation was accompanied
by the removal of competing vegetation (Fig. 1). These results
denote an interaction between P fertilisation and removal of
competing vegetation that was only marginally significant
(F = 2.78, P = 0.10) in the ANCOVA test. Fertilisation with P
had no significant effect on N concentration (Fig. 1) but sig-
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Table 2 – Total number of sprouts per plant, number of sprouts per stump area, and the mean number of sprout
ramifications in the plant for the different treatments one year after clipping. The values of each treatment of the different
variables are represented. (Different letters a, b, c indicate statistically significant differences between different treatments).
Numbers are means ± S.E. Significant differences (P < 0.05) between the treatments are highlighted in bold type. The
significant levels (P) of the two factors and their interaction in the factorial ANOVA design are given in the final three
columns. (Nf = N fertilisation, Pf = P fertilisation, R = Removal of competing vegetation). If ANCOVA was used, it is indicated
by the P value of the cofactor (stump area)
Design: N fertilisation Removal of competing vegetation
Variable
P stump area C
R
N
Sprout number
—
44.7 ± 8.4 (a)
33.6 ± 4.3 (a)
Sprout number
0.0016
0.963 ± 0.184 (a) 0.928 ± 0.155 (a)
−2
cm
Sprout branches
—
2.02 ± 0.25 (a)
2.25 ± 0.32 (a)
Design: P fertilisation · Removal of competing vegetation
Variable
P stump area
C
R
Sprout number
44.7 ± 8.4 (a)
33.6 ± 4.3 (a)
Sprout number
0.0392
0.963 ± 0.184 (a) 0.928 ± 0.155 (a)
cm−2
Sprout branches
0.0032
2.02 ± 0.25 (a)
2.25 ± 0.32 (a)
NR
P for R
P for Nf P
interaction
35.3 ± 7.9 (a)
41.4 ± 8.0 (a)
0.961
0.904 ± 0.431 (a) 0.741 ± 0.180 (a) 0.756
0.112
0.374
0.293
0.168
1.98 ± 0.44 (a)
0.736
0.369
P
PR
P for R
43.5 ± 8.3 (a)
46.7 ± 11.4 (a)
0.992
0.829 ± 0.172 (a) 1.134 ± 0.208 (a) 0.533
P for Pf
0.357
0.507
P interaction
0.683
0.990
3.05 ± 0.69 (a)
0.182
0.139
2.55 ± 0.49 (a)
2.49 ± 0.48 (a)
0.301
0.721
Table 3 – Intensity and importance of the competition between the plants with and without removal of competing
vegetation treatment (R) within the same fertilisation situation: No fertilisation (C and R), N fertilised (N and NR), and P
fertilised (P and PR) on variables of sprouting vigour. The significance level of the difference between the variable values of
C respect to CR, N respect to NR, and P respect to PR calculated in an ANOVA are given in the final three columns
Variable
Competition intensity
(C, R)
(N, NR)
(P, PR)
Leaf biomass
22.85
41.34
–7.91
Stem biomass
13.89
26.73
-22.72
Competition importance
(C, R)
(N, NR)
(P, PR)
(C,R)
P ANOVA
(N,NR)
1.37
2.20
0.002
0.46
0.34
0.81
1.13
0.01
0.66
0.52
0.53
0.69
(P,PR)
Total biomass
18.57
34.63
–13.73
0.005
0.009
1.69
0.006
0.54
0.41
Leaf biomass cm–2
54.91
–0.10
12.84
4.61
0.001
0.005
0.17
0.81
0.68
Stem biomass cm–2
47.46
–16.23
–10.80
3.72
0.003
0.003
0.23
0.73
0.77
Total biomass cm–2
53.22
–12.52
3.11
4.32
0.003
0.0003
0.19
0.77
0.92
Leaf biomass/stem biomass
18.79
28.86
30.01
0.05
3.37
0.11
0.22
0.018
nificantly increased the N and P contents of plant leaves and
stems (up to 50% in leaf P content; Fig. 2). In all of the statistical analyses of N and P contents of leaf and stem, the
stump area accounted for a significant part of the variance.
The plant with largest stumps accumulated the most N and
P. Stump area had a positive effect on N and P content in all
cases. A negative interaction between N fertilisation and removal of competing vegetation was observed in N and P content. This interaction was significant in leaf, stem, and total
biomass P content (Fig. 2).
4.
Discussion
Resprout recruitment in the first year after thinning occurred
gradually rather than suddenly. New sprouts were produced
throughout the year of monitoring. This trend was observed
in all treatments and resprout recruitment did not stop in
any treatment. This behaviour agrees with previous studies
in which successive appearance of resprout cohorts has been
observed (Vilà and Terradas, 1995b). The recruitment of successive resprout cohorts has also been observed in other resprouter species: Arbutus unedo (Mesléard and Lepart, 1989),
12.60
Salvia leucophylla and Artemisa california (Malanson and Westman, 1985) and Eucalyptus sp. (Holland, 1969).
The removal of competing vegetation did not produce important changes in resprouting vigour, although it did have
effects on individual resprout structure and on branch distribution within the plant resprout population. Increases in the
proportion of leaf biomass with respect to stem biomass and
in the number of branches in the resprouts, especially when
P fertilisation was applied, indicate a trend towards lateral
expansion to compete with competitors for space. Greater resprout growth in the P-fertilised plants, especially when the
competing vegetation had been removed, could have increased branching of the resprouts to take advantage of the
greater availability of light and water.
The increase in the Gini coefficient for the number of resprout branches at plant level was a sign of an increase in
the hierarchy of branching in the sprout population after a
decrease in competitive pressure. Although no significant interaction was detected in the ANOVA test (P = 0.29) regarding
the hierarchy of the number of ramifications in the plant
sprout population, P fertilisation was the only factor that
tended to increase this hierarchy when competing vegetation was removed. This effect is probably due to the lack of
ACTA OECOLOGICA
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(2006) 221–232
Table 4 – Means (± S.E.) of the CV (CV, %), the skewness coefficient (g) and the hierarchy coefficient (G) for stem basal
diameter, the height and number of branches of each sprout in the sprout populations of the plants treated and not treated
for each experimental factor. (Different letters a, b, c indicate statistically significant differences between different
treatments). Significant differences (P<0.05) between the treatments are highlighted in bold type. The significant levels (P)
of the two factors and their interaction in the factorial ANOVA design are given in the final three columns. (Nf = N
fertilisation, Pf = P fertilisation, R = Removal of competing vegetation)
Design: N fertilisation Removal of competing vegetation
Variable and
C
CR
N
coefficient
Basal diameter
CV
46.2 ± 3.1 (a)
48.2 ± 3.4 (a)
G
1.07 ± 0.16 (a)
0.88 ± 0.18 (a)
G
0.248 ± 0.016 (a)
0.259 ± 0.018 (a)
Height
CV
46.0 ± 3.2(a)
47.2 ± 2.1 (a)
G
0.760 ± 0.129(a)
0.525 ± 0.103 (a)
G
0.254 ± 0.019 (a)
0.255 ± 0.010 (a)
Branches
CV
140 ± 6 (a)
159 ± 10 (a)
G
1.48 ± 0.12 (a)
1.65 ± 0.18 (a)
G
0.657 ± 0.018 (a)
0.693 ± 0.028 (a)
Design: P fertilisation · Removal of competing vegetation
C
CR
P
Basal diameter
CV
46.2 ± 3.1 (a)
48.2 ± 3.4 (a)
G
1.07 ± 0.16 (a)
0.88 ± 0.18 (a)
G
0.248 ± 0.016 (a)
0.259 ± 0.018 (a)
Height
CV
46.0 ± 3.2 (a)
47.2 ± 2.1 (a)
G
0.76 ± 0.13 (a)
0.53 ± 0.10 (a)
G
0.254 ± 0.019 (a)
0.255 ± 0.010 (a)
Branches
CV
140 ± 6 (a)
159 ± 10 (ab)
G
1.48 ± 0.12 (a)
1.65 ± 0.18 (ab)
G
0.657 ± 0.018 (ab)
0.693 ± 0.028 (ab)
NR
P for R
P for Nf P interaction
55.1 ± 3.8 (a)
1.06 ± 0.32 (a)
0.270 ± 0.025 (a)
44.8 ± 4.5 (a)
0.81 ± 0.17 (a)
0.231 ± 0.023 (a)
0.37
0.28
0.60
0.52
0.84
0.84
0.22
0.55
0.14
50.5 ± 4.9 (a)
0.599 ± 0.140 (a)
0.275 ± 0.026 (a)
45.6 ± 2.1 (a)
0.651 ± 0.153 (a)
0.241 ± 0.014 (a)
0.66
0.40
0.41
0.69
0.95
0.91
0.53
0.85
0.39
155 ± 16 (a)
1.84 ± 0.24 (a)
0.654 ± 0.043 (a)
134 ± 12 (a)
1.60 ± 0.26 (a)
0.604 ± 0.046 (a)
0.41
0.98
0.97
0.60
0.54
0.15
0.96
0.06
0.39
PR
P for R
P for R
P for Pf
P interaction
48.0 ± 2.5 (a)
0.83 ± 0.14 (a)
0.248 ± 0.012 (a)
50.1 ± 2.9 (a)
1.09 ± 0.12 (a)
0.266 ± 0.016 (a)
0.39
0.77
0.27
0.67
0.93
0.94
0.63
0.33
0.06
50.4 ± 2.8 (a)
0.39 ± 0.14 (a)
0.268 ± 0.014 (a)
49.5 ± 2.8 (a)
0.45 ± 0.11 (a)
0.277 ± 0.015 (a)
0.88
0.47
0.59
0.28
0.08
0.28
0.74
0.89
0.23
146 ± 12 (ab)
1.57 ± 0.20 (ab)
0.626 ± 0.044 (a)
172 ± 11 (b)
1.88 ± 0.17 (b)
0.726 ± 0.023 (b)
0.03
0.02
0.04
0.34
0.30
0.98
0.41
0.62
0.29
external competition accelerating the resprout growth, intraplant competition among resprouts, and asymmetrical lateral branching. The positive effects on resprouting vigour
after removal of competing vegetation and fertilisation when
the nutrient is a limiting factor have been observed in other
studies (Reader, 1990; Vilà and Terradas, 1995b), although not
in all (see Matlack et al., 1993). Although it does not provide
any direct evidence (Hara, 1988), the Gini coefficient is
strongly influenced by competition and usually rises when
competition increases (Hutchings, 1986). The positive correlation observed between the height of resprouts and their
corresponding branch numbers indicates that resprout
branching increases when resprouts reach certain heights.
The removal of competing vegetation allows dominant resprouts at plant level to reach this height faster and in this
way the hierarchy of the ramification process in the resprout
populations increases.
The Gini coefficient and the skewness coefficient varied
in different ways according to the variable and experimental
factor studied. These differences, which have also been observed in other experiments (Weiner, 1985), call for caution
when choosing which coefficient to use in the analysis of
the effects of experimental factors on the distribution values
of the population variables. An increase in the hierarchy of
the distribution of one variable does not necessary imply a
parallel increase in the skewness or in the CV.
The P content in the aerial sprouting biomass increased in
response to addition of P. This capacity for accumulation of a
limiting nutrient such as P can provide a competitive advantage during future growth. These results fit the hypothesis of
resprouting advantage providing the capacity to quickly absorb resources after perturbations in response to pulses in
nutrient supplies (Schmid and Bazzaz, 1990; Kroon and
Schieving, 1991). The capacity to increase nutrient content
in biomass during resprouting events coinciding with similar
nutrient increases in soils is a trend that might help prevent
nutrient losses during the first regeneration phase after a
disturbance and help increase water-use efficiency (Sing et
al., 2000; Ruiz-Lozano et al., 2000; Mohammad and Zuraigi,
2003). Such a capacity would enable E. multiflora to resist current and future environmental changes since it allows more
efficient use of available nutrients and improves use of
water, which global circulation models (GCMs) and ecophysiological models predict will become scarcer in the Mediterranean region (IPCC, 2001; Sabaté et al., 2002; Peñuelas et al.,
2004).
The lack of effect of N fertilisation on resprouting vigour
and on nutrient content contrasts with previous reports, in
which N fertilisation increased resprouting vigour and nutrient content in E. multiflora (Vilà and Terradas, 1995a) and in
other resprouting species (Di Tommaso and Aarseen, 1989;
Wilson and Tilman, 1993). This result is especially important
because levels of available N in habitat soil are low compared
to current values reported from natural soils (Malhi et al.,
2003; Dorland et al., 2003), even though the high proportion
of nitrate with respect to ammonium indicates high rates of
228
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(2006) 221–232
Fig. 1 – N and P concentration (mg g−1) (mean ± S.E.) in the resprout leaves and stems of the plants of the two experimental
designs (different letters indicate statistically significant differences between different treatments). C = control, without N
fertilisation and without removal of competing vegetation, N = with N fertilisation and without removal of competing
vegetation, R = without N fertilisation and with removal of competing vegetation, NR = with N fertilisation and removal of
competitive vegetation, P = with P fertilisation and without removal of competing vegetation, PR = with P fertilisation and
with removal of competing vegetation.
Table 5 – Intensity and importance of the competition between the plants with and without neighbours (R) within the same
fertilisation situation: no fertilisation (C and R), N fertilisation (N and NR), and P fertilisation (P and PR) on N and P
concentration. The significance level (P) of the difference between the variable values of C respect to R, N respect to NR, and
P respect to PR calculated in an ANOVA are presented in the last three columns
Variable
(C, R)
Competition intensity
(N, NR)
(P, PR)
N in leaves
6.66
4.13
-–1.84
N in stems
–5.22
1.59
P in leaves
–3.90
P in stems
12.52
(C, R)
Competition importance
(N, NR)
(P, PR)
(C, R)
P ANOVA
(N, NR)
(P, PR)
3.60
1.29
0.34
0.048
0.42
5.12
2.31
4.89
0.04
5.19
0.16
0.79
0.10
4.22
19.12
2.60
5.21
19.33
0.31
0.15
0.04
-8.72
27.19
13.40
5.23
30.81
0.017
0.16
<0.0001
ACTA OECOLOGICA
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(2006) 221–232
229
Fig. 2 – Total N and P content of leaf, stem and aerial portions (mg per , mean ± S.E.) of plant resprout population (different
letters indicate statistically significant differences between different treatments). C = control, without N fertilisation and
without removal of competing vegetation, N = with N fertilisation and without removal of competing vegetation,
R = without N fertilisation and with removal of competing vegetation, NR = with N fertilisation and removal of competitive
vegetation, P = with P fertilisation and without removal of competing vegetation, PR = with P fertilisation and with removal
of competing vegetation.
mineralisation. Nevertheless, in accordance with other experiments conducted at this same site that have not observed any effects of N fertilisation on growth and nutrient
content of other species, this lack of effect of N fertilisation
is probably the result of rapid mineralisation of N in these
calcareous soils (Sardans et al., 2004). Additional N supply increased N concentration in the leaves and in the stems of the
resprouts, but slightly reduced the total biomass of the popu-
230
ACTA OECOLOGICA
lation of the plant sprouts. The overall effect was that the N
and P contents of the plants fertilised with N did not change.
This slight reduction in growth in response to N fertilisation is
not an exceptional event and has been observed previously in
other studies. For example, high levels of N fertilisation
(400 kg ha–1) in a soil already rich in N decreased the growth
of Zea mays, even though this species typically grows in nutrient rich soils (Pozo et al., 1992). Similarly, in a fertilisation experiment with stands of Picea abies, an additional supply of N
and P had a negative effect (–10%) on radial growth (Picard et
al., 1999). However, the suggested reason for the negative effect of increased nitrogen availability, the increased growth of
the competing vegetation (Skrindo and Okland, 2002), does not
stand in this case given our experimental conditions (the continuous “clearing” of a 1 m2 circle surrounding the plants).
Thus, further research into this question is warranted in order
to gain better understanding of this phenomenon.
E. multiflora showed only a small capacity to increase production of new resprouts and general resprout vigour as a response to fertilisation. Stronger effects were observed in nutrient content. Plants fertilised with N and P increased their
concentrations of these nutrients in resprout biomass,
although only in plants fertilised with P were these increases
translated into increases of absolute P content in biomass.
The positive effects of P fertilisation on P content were principally due to P concentration increases and, to a lesser extent, to the effects of sprout vigour during the first year after
fertilisation. The removal of competing vegetation increased
the lateral expansion of the plant resprout population and
increased allocation to photosynthetic structures when P
was applied. The removal of competing vegetation increased
P concentrations in stems and had a positive effect on biomass and nutrient content. These results show a capacity
to increase nutrient capture in response to changes in nutrient supplies during the first stages of resprouting, an ability
that is modulated by the presence of competing vegetation.
Nevertheless, a single year after clipping may not be long enough to detect the full effects of nutrient addition and the
removal of competing vegetation on resprouting vigour.
These trends in resprouting and regeneration capacity may
be critical for specific persistence in Mediterranean forests
and shrublands in the near future in light of continued disturbance. Steeper nutrient gradients (Peñuelas and Filella,
2001), together with warming trends (Piñol et al., 1998; Peñuelas et al., 2002) and a downward trend in precipitations
(Esteban-Parra et al., 1998), will play a significant role in the
capacity of Mediterranean plant species to capture and use
nutrients. In fact, in an altitudinal gradient it has been found
that the growth of plants of the genus Erica is more correlated to nutrient availability than to climatic conditions
(Hicks et al., 2000).
Acknowledgements
This research was supported by Spanish MEC grants AMB
95-0247, REN 2003-04871/GLO and CGL2004-01402/BOS and by
European Union project ALARM (Contract 506675). Additional
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partial funding was provided by a Fundación Banco Bilbao
Vizcaya 2004 grant.
R E F E R E N C E S
Aarseen, L.W., Epp, G.A., 1990. Neighbour manipulation in
natural vegetation: a review. J. Veg. Sci. 1, 13–30.
Bendel, R.B., Higgins, S.S., Teberg, J.E., Pyke, D.A., 1989. Comparison of Skewness coefficient, coefficient of variation,
and Gini coefficient as inequality measures within populations. Oecologia 78, 394–400.
Berstson, G.M., Weiner, J., 1991. Size structure of populations
within populations: leaf number and size in crowed and
uncrowed Impatiens pallida individuals. Oecologia 85, 327–
331.
Carreira, J.A., Arevalo, J.R., Niell, F.X., 1996. Soil degradation
and nutrient availability in fire-prone Mediterranean
shrublands of southern eastern Spain. Arid Soil Res. and
Rehabilitation 10, 53–64.
Cruz, A., Moreno, J.M., 2001. Lignotuber size of Erica australis
and its relationship with soil resources. J. Veg. Sci. 12, 373–
384.
Di Tommaso, A., Aarseen, L.W., 1989. Effect of nutrient level
on competition intensity in the field for three coexisting
grass species. J. Veg. Sci. 2, 513–522.
Dorland, E., Bobbnik, R., Messelinki, J.H., Verhoeven, J.T.A.,
2003. Soil ammonium accumulation after sod cutting
hampers the restoration of degraded wet heatlands. J
Appl. Ecol. 40, 804–814.
Ellis, B.A., Kummerow, J., 1989. The importance of N2 fixation
in Ceanothus seedlings in early post-fire Chaparral. In:
Keely, S.C. (Ed.), The California Chaparral: Paradigms Reexaminated. Science Series, No 34. Natural History Museum of LA County, pp. 115–116.
Esteban-Parra, M.J., Rodrigo, F.S., Castro-Díez, Y., 1998. Spatial
and temporal patterns of precipitation in Spain for the
period 1880–1992. Int J Climato 18, 1557–1574.
Gimeno-García, E., Andreu, V., Rubio, J.L., 2000. Changes in
organic matter, nitrogen, phosphorus and cations in soil
as a result of FIRE and water erosion in a Mediterranean
landscape. Eur. J. Soil Sci. 51, 201–211.
Grime, J.P., 1977. Evidence for the existence of three primary
strategies in plants traits and its relevance to ecological
and evolutionary theory. Am. Nat. 111, 1169–1194.
Hanes, T.L., 1971. Succession after fire in the chaparral of
southern California. Ecol. Monogr. 41, 27–52.
Hara, T., 1988. Dynamics of size structure in plant populations. Trees 3, 129–133.
Hicks, W.K., Leith, I.D., Woodne, S.J., Fowler, D., 2000. Can the
foliar nitrogen concentrations of upland vegetation be
used for predicting atmospheric of afroalpine ecosystems.
Environ. Poll. 3, 367–376.
Holland, P.G., 1969. Weight dynamics of Eucalyptus in the malee vegetation of Southern Australia. Ecology 50, 212–219.
Hutchings, M.J., 1986. The structure of plant populations. In:
Crawley, M.J. (Ed.), Plant Ecology. Blackwell Scientific Publications, New York, pp. 97–136.
IPCC (2001) Climate Change 2001: The Scientific Basis. Contribution of Working Group I, 2001. Third Assessment Report
of Intergovermental Panel on Climate Change. In: Hougton, J.T., Dung, Y., Griggs, D.J., Noguer, M., Van der Linden,
P.J., Dui, X., Maskell, K., Johnson, C.A. (Eds.). Cambridge
University, Press, Cambridge.
Jackson, D.A., Harvey, H.H., Somers, K.M., 1990. Ratios in
aquatic sciences: statistical shortcomings with mean
ACTA OECOLOGICA
depth and morphoedaphic index. Canadian J. Fisheries &
Aquatic Sci. 47, 1788–1795.
Kroon, H., Schieving, F., 1991. Resource allocation patterns as
a function of clonal morphology: a general model applied
to a foraging clonal plant. J. Ecol. 79, 519–530.
Kutiel, P., Kutiel, H., 1989. Effects of a wildfire on soil nutrients and vegetation in an Aleppo pine forest, on Mont
Carmel, Israel. Pirineos 134, 59–73.
Kutiel, H., Maheras, P., Guika, S., 1996. Circulation and extreme rainfall conditions in the Eastern Mediterranean
during the last century. Int. J. Climatology. 16, 72–92.
Liermann, M., Steel, A., Rosing, M., Guttorp, P., 2004. Random
denominators and the analysis of ratio data. Environ. Ecol.
Statistics 11, 55–71.
Llorens, L., Peñuelas, J., Estiarte, M., 2003. Ecophysiological
responses of two Mediterranean shrubs, Erica multiflora
and Globularia alypum, to experimental drier and warmer
conditions. Physiol. Plantarum 119, 231–243.
Llorens, L., Peñuelas, J., Estiarte, M., Bruna, P., 2004. Contrasting growth changes in two dominant species of a Mediterranean shrubland submitted to experimental drought and
warming. Ann. Bot 94, 843–853.
Lloret, F., Verdú, M., Flores-Hernández, N., Valiente-Baunet,
A., 1999. Fire and resprouting in Mediterranean ecosystems: insights from an external biogeographical region,
the mexical shrubland. Am. J. Bot. 86, 1655–1661.
Lloret, P.L., López-Soria, L., 1993. Response of Erica multiflora
after experimental fire treatments. J. Veg. Sci. 65, 345–363.
Malanson, G.P., Westman, W.E., 1985. Postfire succession in
Californian coastal sage shrub: the role of continual basal
sprouting. Am. Mid. Nat. 113, 309–318.
Malhi, S.S., Harapiak, J.T., Nyborg, M., Gill, K.S., Monreal, C.M.,
Gregorich, E.G., 2003. Light fraction organic N, ammonium,
nitrate and total N in a thin Black Chernozenic soil under
bromegrass after 27 annual applications of different N
rates. Nut. Cycl. Agrosystems 65, 201–210.
Matlack, G.R., Gibson, D.J., Good, R.E., 1993. Regeneration of
the shrub Gaylussacia baccato and associated species after
low-intensity fire in an Atlantic coastal plain forest. Am. J.
Bot. 80, 119–126.
Mayor, X., Rodà, F., 1994. Effects of irrigation and fertilisation
on stem diameter growth in a Mediterranean holm oak
forest. Forest Ecol. Manag. 68, 119–126.
Mesléard, F., Lepart, J., 1989. Continuous basal sprouting from
a lignotuber: Arbutus unedo L. And Erica arborea L., as woody Mediterranean examples. Oecologia 80, 127–131.
Mohammad, M.J., Zuraigi, S., 2003. Enhancement of yield and
nitrogen and water use efficiency by nitrogen drip-fertilization of garlic. J. Plant Nutrition 26, 1749–1766.
Mooney, H.A., Dunn, E.L., 1970. Convergent evolution of Mediterranean-climate evergreen sclerophyll shrubs. Evolution 24, 292–303.
Orshan, G., 1989. Plant Phenomorphological Studies in Mediterranean Type Ecosystems. Kluwer Academic Publishers,
Dordrecht.
Pausas, J.G., 2004. Changes in fire and climate in the eastern
Iberian Peninsula (Mediterranean basin). Climate Change
63, 337–350.
Peltzen, D.A., Kochy, M., 2001. Competitive effects of grasses
and woody plants in mixed-grass praire. J. Ecol. 89, 519–
527.
Peñuelas, J., Filella, I., 2001. Herbaria century record of increasing eutrophication in Spanish terrestrial ecosystems.
Global Change Biol. 7, 427–433.
Peñuelas, J., Filella, I., Comas, P., 2002. Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Global Change Biol. 8, 531–544.
29
(2006) 221–232
231
Peñuelas, J., Boada, M., 2003. A global change-induced biome
shift in the Montseny mountains (NE Spain). Global
Change Biol. 9, 131–140.
Peñuelas, J., Sabaté, S., Filella, I., Gracia, C., 2004. Efectos del
cambio climático sobre los ecosistemas terrestres: observación, experimentación y simulación. In: Valladares, F.
(Ed.), Ecología del bosque mediterráneo en un mundo
cambiante. Naturaleza y Parques Nacionales. Ministerio
de Medio Ambiente, Madrid, pp. 425–460.
Picard, J.F., Becker, M., Nys, C., Duponey, J.L., Aussenac, G.,
1999. Medium term radial growth of Norway spruce and
beech in relation to application of fertilizers and/or soil
amendments: a dendroecological analysis. Rev. Forestiere
Francoise 51, 197–218.
Piñol, J., Terrades, J., Lloret, F., 1998. Climate warning, wildfire
hazard, and wildfire occurrence in coastal eastern Spain.
Climate Change 38, 345–357.
Pozo, C., Cruces, C., Ramos, J.M.R., García del Moral, L.F., 1992.
Depresión del rendimiento del maíz causado por altas
concentraciones de N residual en el suelo. Suelo y Planta
2, 617–628.
Prevost, M., 1994. Scalping and burning of Kalmia angustifolia
(Ericaceae) litter: effects on Picea mariana establishment
and ion leaching in a greenhouse experiment. Forest
Ecol. Manag. 63, 199–218.
Reader, R.J., 1990. Competition constrained by low nutrient
supply: an example involving Hieracium floribundum
Wimm and Grab. (Compositae). Funct. Ecol. 4, 573–577.
Romanya, J., Casals, P., Vallejo, V.R., Cramer, W., 2001. Shortterm effects of fire on soil nitrogen availability in Mediterranean grasslands and shrublands growing in old fields.
Forest Ecol. Manag. 147, 39–53.
Ruiz-Lozano, J.M., Collados, C., Barea, J.M., Azcón, R., 2000.
Arbuscular mycorrhizal symbiosis can alleviate droughtinduced nodule senescence in soybean plants. New Phytol. 151, 493–502.
Sabaté, S., Gracia, C., Sánchez, A., 2002. Likely effects of climate change on growth of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in
the Mediterranean region. Forest Ecol. Manag. 162, 23–37.
Sardans, J., 1997. Respostes de 4 espècies llenyoses mediterrànies a diferent disponibilitat d’aigua i nutrients. Ph.D.
Thesis. Universitat Autònoma de Barcelona, Bellaterra.
Sardans, J., Rodà, F., Peñuelas, J., 2004. Phosphorus limitation
and competitive capacities of Pinus halepensis and Quercus
ilex ssp. rotundifolia on different soils. Plant Ecol. 174, 305–
317.
Schmid, J., Bazzaz, F.A., 1990. Plasticity in plant size and architecture in rhizome-derived vs. seed-derived Solidago
and Aster. Ecology 71, 523–535.
Sen, A., 1973. On Economic Inequality. Clarendon Press, Oxford.
Sing, D.K., Sale, P.W.G., Pallaghy, C.K., McKenzie, B.M., 2000.
Phosphorus concentrations in the leaves of defoliated
white clover affect abscisic acid formation and transpiration in drying soil. New Phytol. 146, 249–259.
Skrindo, A., Okland, R.H., 2002. Effects of fertilisation on understory vegetation in a Norwegian Pinus sylvestris forest.
Appl. Veg. Sci. 5, 167–172.
Soto, B., Basanta, R., Diaz Fierro, F., 1997. Effects of burning on
nutrient balance in an area of garse (Ulex parviflorus L.)
scrub. Catena 36, 283–302.
Specht, R.L., 1973. Structure and functional response ecosystems in the Mediterranean climate of Australia. In: di Castri, F., Mooney, H.A. (Eds.), Mediterranean-Type Ecosistems. Origin and Structure. Chapman and Hall, London,
pp. 113–120.
232
ACTA OECOLOGICA
Thomas, A.D., Walsh, R.P.D., Shakesby, R.A., 1999. Nutrient
losses in eroded sediment alter FIRE eucalyptus and pine
forest in the wet Mediterranean environmental of northern Portugal. Catena 36, 283–302.
Tilman, D., 1982. Resource Competition and Community
Structure. Princeton University Press, Princeton, New
York.
Tilman, D., 1990. Constrains and trade-off: toward a predictive theory of competition and succession. Oikos 58, 3–15.
Vilà, M., Terradas, J., 1995a. a. Effects of nutrient availability
and neighbours on shoot growth, resprouting and flowering of Erica multiflora. J. Veg. Sci. 6, 411–416.
Vilà, M., Terradas, J., 1995b. b. Effects of competition and disturbance on the resprouting performance of the Mediterranean shrub Erica multiflora L. (Ericaceae). Am. J. Bot. 82,
230–234.
Vilà, M., Lloret, F., 1996. Herbivory and neighbour effects on
the sprout demography of the Mediterranean shrub Erica
multiflora (Ericaceae). Acta Oecol. 17, 127–138.
Vilà, M., 1997. Effect of root competition and shading on resprouting dynamics of Erica multiflorea L. J. Veg. Sci. 8, 71–
80.
29
(2006) 221–232
Vilà, M., Stoll, P., Weiner, J., 1998. Effects of Rosmarinus officinalis neighbours on resprouting of Erica multiflora individuals. Plant Ecol. 136, 167–173.
Vilà, M., Terradas, J., 1998. Neighbour effects on Erica multiflora (Ericaceae) reproductive performance after clipping.
Acta Oecol. 19, 139–145.
Vitousek, P.M., Aber, J.D., Howarth, R.W., 1997. Human alteration of global nitrogen cycle: sources and consequences.
Ecol. Appl. 7, 737–750.
Weiner, J., Solbrig, O.T., 1984. The meaning and measurement
of size hierarchies in plant populations. Oecologia 61, 334–
336.
Weiner, J., 1985. Size hierarchies in experimental populations
of annual plants. Ecology 66, 743–752.
Welden, C.W., Slauson, W.L., 1988. The intensity of competition versus its importance: an overlooked distinction and
some implications. The Quarterly Review of Biology 61,
23–44.
Wilson, S.D., Tilman, D., 1993. Plant competition and resource
availability in response to disturbance and fertilisation.
Ecology 74, 599–611.