Geoderma 166 (2011) 135–144

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Geoderma
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / g e o d e r m a

The effect of lime and compost amendments on the potential for the revegetation of
metal-polluted, acidic soils
Salomé Córdova a, Alexander Neaman a, b,⁎, Isabel González c, Rosanna Ginocchio d, Pinchas Fine e
a
Facultad de Agronomía, Pontificia Universidad Católica de Valparaíso, Quillota, Chile
b
Centro Regional de Estudios en Alimentos Saludables (CREAS), Región de Valparaíso, Chile
c
Doctorado en Geografía, Planificación Territorial y Gestión Ambiental, Universitat de Barcelona, España, Spain
d
Unidad de Fitotoxicidad y Fitorremediación, Centro de Investigación Minera y Metalúrgica, Santiago, Chile
e
Institute of Soil, Water and Environmental Sciences, Agricultural Research Organization, Volcani Center, Bet Dagan, Israel

a r t i c l e i n f o a b s t r a c t

Article history: The revegetation of soils affected by the historic pollution of an industrial complex in central Chile was
Received 27 October 2010 studied. Spontaneous and assisted revegetation and changes in the physicochemical properties of the soils
Received in revised form 28 June 2011 were evaluated in field plots that were amended with lime or lime + compost. Lime had no effect on plant
Accepted 23 July 2011
productivity in comparison with the control, whereas the incorporation of lime + compost into the soil
Available online 19 August 2011
increased the plant cover and aboveground biomass. The application of lime + compost increased the plant
Keywords:
productivity of Chrysanthemum coronarium (a species sensitive to the atmospheric emissions from the
Spontaneous revegetation industrial complex), thus showing effective in situ stabilization of soil contaminants. Regression analyses
Assisted revegetation suggested that the plant response was due to the increase in the soil organic matter content rather than to the
Puchuncaví Valley increase in the soil pH. The aboveground biomass and plant cover did not differ under the spontaneous and
Ventanas industrial complex assisted revegetation regimes. The native soil seed bank was sufficient for attainment of the proper plant
Phytostabilization cover and biomass production after the application of the soil amendments. Although the pCu 2+ in the
Phytoremediation amended soils was 4 orders of magnitude higher than in the unamended control, the shoot Cu concentration
was similar among most of the combinations of plant species and amendments.
© 2011 Elsevier B.V. All rights reserved.

1. Introduction (Pierzynski, 1997). In the more severe circumstances, where plant

The semiarid Mediterranean ecosystem of the Puchuncaví Valley
in the coastal area of central Chile was exposed to atmospheric
deposition of sulfur dioxide (SO2) and metal-rich particles from the
Ventanas industrial complex from 1964 to 1992 (Folchi, 2006). After
1992, the complex incorporated a range of technologies to reduce the
atmospheric emissions of SO2 and particulate matter to meet the new
Chilean environmental regulations. However, the soils surrounding
the industrial complex had accumulated Cu and other elements at
high concentrations, were acidified and strongly eroded and had lost
much of their native vegetative cover (De Gregori et al., 2003;
Ginocchio, 2000; Neaman et al., 2009).
Soil acidification and metal pollution inhibit the growth of wild
plants and microorganisms and restrict agricultural activities, partic-
ularly when bioavailable metal concentrations are above the tolerance
thresholds of organisms (Adriano, 2001). These impacts may also
increase human and animal exposure to metals through food chain
transfer, inhalation of wind-blown dust, or direct ingestion of soil
⁎ Corresponding author.
E-mail address: alexander.neaman@ucv.cl (A. Neaman).
growth is strongly inhibited, off-site contaminant migration might
occur through both increased soil erosion and the leaching of metals
into the groundwater (Vangronsveld and Cunningham, 1998).
Reduction of the environmental risks posed by acidic and metal-
polluted soils, such as the ones present in the Puchuncaví Valley,
requires affordable and effective remediation alternatives, particular-
ly at large spatial scales. In this scenario, in situ immobilization,
defined as the reduction of the concentration of bioavailable metals in
the soil solution by adding amendments without altering the soil
structure (Macnair et al., 2000), has been suggested as a cost-effective
alternative for metal-polluted soils (Glass, 1999; Lasat, 2000). The
amendments do not remove the metals from the soil, but transform
them into less soluble or insoluble forms (Macnair et al., 2000; Mench
et al., 2003) through the mechanisms of adsorption, complexation or
co-precipitation (Kumpiene et al., 2008). As a result, soil quality is
improved. A preliminary laboratory assessment to identify adequate
soil amendments for the in situ immobilization of metals in the
Puchuncaví Valley demonstrated the effectiveness of a mixture of
lime and compost for improving the physicochemical characteristics
and reducing the soluble fractions of Cu and other metals in the soils
of the valley (Goecke et al., 2011). The improvement of soil quality
resulted in increased productivity of Lolium perenne (ryegrass) plants,

0016-7061/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.geoderma.2011.07.022
136 S. Córdova et al. / Geoderma 166 (2011) 135–144
a bioindicator of Cu toxicity. Accordingly, the study postulates that the
application of lime and compost is likely to improve the potential for
the revegetation of metal-polluted, acidic soils.
Phytostabilization is another in situ metal immobilization tech-
nique (Mench et al., 2003; Tordoff et al., 2000; Vangronsveld et al.,
1995). In metal-polluted soils that did not undergo prior chemical
metal stabilization, successful phytostabilization requires metal-
tolerant plant species that immobilize metals through absorption
and accumulation by roots, adsorption onto roots, and/or precipita-
tion within the rhizosphere (Arienzo et al., 2004). Effective phytost-
abilization also requires that the plants posses an extensive root
system, and that the metals are not translocated into aboveground
tissues (Rizzi et al., 2004; Simon, 2005).
Phytostabilization of metal-polluted sites can rely on spontaneous
revegetation of native plants from the soil seed bank (Álvarez et al.,
2003; Conesa et al., 2007; Madejón et al., 2006), or it can be by assisted
revegetation, employing seeding and/or transplanting of resistant
plant species (Alvarenga et al., 2008; Arienzo et al., 2004; Clemente
et al., 2005). Although the former is less costly, the latter offers quicker
and more effective revegetation with likely more resistant plant
species, and it might also be achieved without physicochemical pre-
conditioning of the soil. Nonetheless, spontaneous revegetation from
the soil seed bank would depend on the abundance and quality of the
seeds present in the topsoil and the capability of local plant species to
tolerate the conditions. In metal-polluted, acidic soils, the addition of
soil amendments may be required as the plants represented in the soil
seed bank are not necessarily tolerant to the deteriorated site
conditions. In the case of the Puchuncaví Valley, the abundance and
spatial distribution of adult plants and the variability of the soil seed
bank both decline with decreasing distance from the industrial
complex (Ginocchio, 2000). This exemplifies the diminishing capacity
of the ecosystem for spontaneous regeneration. Therefore, at least in
the short-term, assisted revegetation might better enhance vegetation
productivity and soil coverage compared with spontaneous vegetation
development.
Fig. 1. Location of the experimental field at Los Maitenes, Puchuncaví valley, central Chile.
In this study, we tested a cost-effective alternative for site re-
mediation of the metal-polluted, acidic soils in the Puchuncaví Valley,
which is based on the use of soil amendments for in situ immobilization
of metals and on phytostabilization with spontaneous and seeded/
planted species. The specific objectives were (i) to evaluate the effects of
lime with and without compost on the physicochemical characteristics
of the soil and on vegetation productivity and (ii) to compare vegetation
productivity under assisted and spontaneous revegetation regimes.
2. Materials and methods
2.1. Study area
The study took place at the Los Maitenes area in the Puchuncaví
Valley, 1 km southeast of the Ventanas industrial complex (Figure 1),
where the highest soil concentrations of Cu, Pb, Zn, Cd and As (arsenic
will be referred to as “metal” in the following discussion) and the
lowest soil pH measurements have been recorded (Ginocchio et al.,
2004; González et al., 2008; González and Bergqvist, 1986; González
and Ite, 1992). For example, total soil Cu concentrations reached
680 mg kg −1, a concentration that might be toxic to plants (Fernándes
and Henríques, 1991), particularly as Cu bioavailability is high
(Neaman et al., 2009) in this acidic soil (pH in KNO3 of 3.9–5.9;
González et al., 2008). The soils at Los Maitenes also had lower organic
carbon and nitrogen contents than the background soils of the valley
(Ginocchio, 2000).
2.2. Experimental plot
In January 2009, a 754 m 2 experimental field (29 m × 26 m) was
set up at Los Maitenes (UTM 268.461 E and 6.371.841 N; Figure 2) on a
slope of approximately 10%. Because topographical position might
have influenced the spatial distribution of the metals (Ginocchio et al.,
2004), the experimental field was divided into three blocks with
respect to topographical position: low, medium, high (Figure 2). The
 S. Córdova et al. / Geoderma 166 (2011) 135–144 137

Fig. 2. Schematic distribution of blocks (left) according to the topographical position (low, medium, and high) and location of experimental treatments (right). bn indicates the
number of block. 0 = unamended control, L = lime, LCO = lime + compost.

experimental field was fenced with wire-mesh to prevent the
entrance of cattle and wild herbivores present in the study area. The
soil was tractor-plowed to 15-cm depth. Each block was subdivided
into 6 plots of 24 m 2 (4 m × 6 m), separated from each other by 1-m
wide aisles. A 20 cm-height polystyrene mesh was placed along the
perimeter of each plot to prevent inter-plot contamination. The
topsoil (the top 0–15 cm) of all of the plots was sampled (one
composite sample per plot).
The soil treatments consisted of two factors: amendment type and
revegetation regime. Within each block, the plots were randomly
allotted into six treatments (Figure 2): (1) Unamended control (0) +
assisted revegetation; (2) Unamended control (0) + spontaneous re-
vegetation; (3) lime (L) + assisted revegetation; (4) lime (L) +
spontaneous revegetation; (5) lime + compost (LCO) + assisted re-
vegetation; and (6) lime + compost (LCO) + spontaneous revegeta-
tion. Assisted revegetation also included the natural development of
the spontaneous species present in the soil seed bank at the site. The
amendments were applied in March 2009 and plowed to a depth of
15 cm. The bulk density of the soil was 1.48 g cm −3 (AENOR, 2001).
Calcium hydroxide (Ca(OH)2), which was used as liming agent
(Neaman et al., 2009; Stuckey et al., 2009), was applied at a rate of
3 g kg −1 soil (6.7 t ha −1). This rate was determined by a preliminary
laboratory test performed with the objective of adjusting the pH of
the saturated paste extract of the study soil up to approximately 7
following incubation for 48 h at 60 °C (after Sadzawka et al., 2006).
The compost was obtained from a local farm. It contained 56% organic
matter (OM) and 1.9% total nitrogen; it had a C/N ratio of 16, a pH of
7.5 and an electrical conductivity (EC) of 10 dS m −1 (at a 1:5 extrac-
tion ratio), as determined by routine methods from Sadzawka et al.
(2006). The compost application rate (on a dry weight basis) was
60 g kg −1 soil (133 t ha −1), which is within the range recommended
by the U.S. EPA (2007) for the remediation of metal-polluted soils.
After the application of the amendments, 70 mm of water was applied
by drip irrigation for one month, on both the spontaneous and
assisted revegetation plots. The pH of the irrigation water was 7.0, and
the EC and the sodium adsorption ratio (SAR) were 0.4 dS m −1 and
0.8 (meq/L) 0.5, respectively.
One month after the application of the amendments, the following
six species were planted/sown on the plots designated for assisted
revegetation: Chrysanthemum coronarium L., L. perenne L., Muehlen-
beckia hastulata (J.E. Sm.) I.M.Johnst., Oenothera picensis Phil., Rumex
acetosella L., Solidago chilensis Meyen. The selection criteria for the
species, the propagation mechanism and the quantity transplanted/
sown are shown in Table 1. The transplanting/seeding rate was
chosen on the basis of the local availability of propagules. All selected
species were locally available in non-polluted areas of the Puchuncaví
Valley; the propagules (seeds, ramets, cuttings, and seedlings) were
hand-collected for the study as indicated in Table 1.

Table 1
Plant species selected for assisted revegetation, their main characteristics and propagation method.

Plant species General description Selection criteria Propagation method Rate/

m−2

Chrysanthemum Wild-grown herbaceous annual plant A potential foraging species (Sulas et al., 1999). Sowing of seeds collected from a 2.3 g
coronarium that reseeds easily (Riedemann and Species sensitive to atmospheric emissions from site 3 km south of Los Maitenes
Aldunate, 2004) the Ventanas industrial complex (Ginocchio, 1997).
Therefore, it is a good indicator of successful
phytostabilization
Lolium perenne Perennial gramineae (Santibáñez et al., Presents low Cu translocation factor (Santibáñez Sowing of commercial seeds 13.6 g
2008) et al., 2008). Therefore, is a good candidate for
phytostabilization
Muehlenbeckia Native perennial woody bush of Fast growing and used as ground cover (Riedemann Planting of 10 cm cuttings using Keriroot 2.3
hastulata ornamental value (Riedemann and and Aldunate, 2004) (commercial rooting promoter). Cuttings seedlings
Aldunate, 2004) were collected from a site 3 km south of
Los Maitenes
Oenothera Fast growing herbaceous biannual plant Considered a good candidate for phytoremediation in Planting of seedlings collected in Los 2.3
picensis (Riedemann and Aldunate, 2004) Chile (González et al., 2008) Maitenes seedlings
Rumex Perennial rhizomatosous herb (Kil et al., Propagates using ramets, generating greater ground Direct transplanting of ramets from a site 2.3
acetosella 1997) cover (Kil et al., 1997) located 3 km south of Los Maitenes ramets
Solidago Herbaceous rhizomatosous perennial Very fast growing, easy propagation via ramets Planting of ramets from a site located 2.3
chilensis plant (Riedemann and Aldunate, 2004) (Riedemann and Aldunate, 2004) 3 km south of Los Maitenes ramets
138 S. Córdova et al. / Geoderma 166 (2011) 135–144
The spatial distribution of the species selected for assisted re-
vegetation is shown in Fig. 3. Each plot was subdivided into six sub-
plots of 2 m × 2 m, each of which was used for the sowing/planting of
one species. The final planting/sowing was completed after dividing
each sub-plot into nine sectors of 0.66 m × 0.66 m (0.44 m 2 each),
which allowed for a more homogeneous distribution of the plants
(Figure 3). Thus, the hierarchical order within the experimental
design was the following: the experimental field was divided into
three blocks; each block was divided into 6 plots of 4 m × 6 m; each
plot was divided into six sub-plots of 2 m × 2 m; each sub-plot was
divided into nine sectors of 0.66 m × 0.66 m.
The plots were irrigated immediately after planting and maintained
for a month at a rate of 10 mm/week −1. The spontaneous revegetation
plots were not irrigated during this month. Overall, the natural
precipitation was approximately 300 mm year−1 (Cosio et al., 2007).
In September 2009, five months after the application of the amend-
ments, the topsoil (0–15 cm) was sampled in all of the plots (one
composite sample per plot) and the soil physicochemical characteristics
were evaluated.
2.3. Physicochemical characterization of the soils
The soil samples were dried at 40 °C and sieved through a 2-mm
mesh. The soil samples were digested in boiling nitric acid followed by
perchloric acid addition (Maxwell, 1968). The total concentrations of Cu,
Pb and Zn were determined by atomic absorption spectrophotometry
(AAS; GBC, model 902, Dandenong, Victoria, Australia). Quality was
assured by similarly digesting in duplicate samples of a certified re-
ference soil sample (GRX-2) obtained from the United States Geological
Survey. The organic matter (OM) content was determined by wet
combustion with sodium dichromate and sulfuric acid without heat
application (Sadzawka et al., 2006). The texture was determined using a
simplified hydrometer method (Sheldrick and Wang, 1993). The water
content at −0.33 bar was determined according to Richards (1965). The
electrical conductivity (EC) was determined in saturated paste extracts
(Sadzawka et al., 2006).
The soil nutrient availability was determined by routine methods
used in Chile as described by Rodríguez (1992) and Sadzawka et al.
(2006). Specifically, the available Ca and Mg were extracted with 1 M
CH3COONH4 at pH 7.0 and determined by AAS after addition of
lanthanum. The available K was determined by atomic emission
spectrophotometry in the same extract. The available P was deter-
mined by the Olsen method (extraction with 0.5 M NaHCO3 at pH 8.5)
and colorimetrically measured with molybdenum blue. The available
Fig. 3. Schematic distribution of cultivated plant species for assisted revegetation and random sampling scheme for determining plant responses using 0.66 m × 0.66 m frame
(dashed squares).
N (the sum of N–NO3− and N–NH4+) was extracted by 2 M KCl and
determined by titration following NH3 distillation.
The exchangeable Cu and pH were determined in 0.1 M KNO3
extract at a 1:2.5 soil:liquid ratio (Stuckey et al., 2009) following
reciprocal shaking for 1 h, centrifugation at 9000 rpm for 10 min and
filtration through 8-μm filter paper. The copper activity in the 0.1 M
KNO3 extract was measured with a Cu 2+ ion-selective electrode
(Orion 96–29 ionplus). The electrode was calibrated using a buffer
solution of iminodiacetic acid (Rachou et al., 2007).
2.4. Plant response variables
The plant cover and aboveground biomass were measured in
November 2009, seven months after the application of the amend-
ments. Two random sectors were sampled within each sub-plot, with
a total of 12 sectors sampled per plot (Figure 3). Sectors were chosen
by randomly placing a frame made of polyvinyl chloride (PVC)
(0.66 m × 0.66 m; 0.44 m 2). The shoots of all of the plants (spontane-
ous and sown/planted) within the frame were sampled. Elemental
analysis was performed only on the shoots of the sown/planted
species (assisted revegetation).
2.4.1. Plant cover
To determine plant cover in each of the sectors, another frame,
subdivided with strings at 0.11 m × 0.11 intervals, was placed on top
of the first one. The perpendicular intersections of these strings
generated 25 intersection points. The numbers of intersecting points
which overlaid bare soil, a spontaneous species or a cultivated species
(in the assisted vegetation treatment) were recorded. This method
was adapted from Goldsmith et al. (1986). The weighted cover per
species was then estimated, considering that 300 points (25 points
per sector × 12 sectors per plot) is equivalent to 100% coverage of the
plot (Tables 4 and 5). To compare the plant cover of the different
cultivated species (assisted revegetation), an estimate of the weighted
cover per species was also made, considering that 50 points (25 points
per sector × 2 sectors of each species per plot) is equivalent to 100%
coverage of the species in the plot (Table 6).
2.4.2. Aboveground biomass
In each of the 12 monitored sectors per plot, all of the plants within
the frame were cut at their bases and each species was collected
separately for laboratory analyses. The shoots of the cultivated species
were then washed in the following sequence: tap water, 0.1 M HCl,
distilled water, 0.05 M EDTA, and distilled water (Steubing, 1982);
 S. Córdova et al. / Geoderma 166 (2011) 135–144
excess water was removed with a paper towel. Spontaneous species
were combined and were not washed before drying. Subsequently, all
shoot samples were dried at 70 °C for 48 h and weighed, providing
biomass on a dry weight (dw) basis for each cultivated species, the
sum of all spontaneous species, and the total biomass per sector and
per plot. For each revegetation regime, the average and standard
deviation of the total plant aboveground biomass per plot was
calculated. The aboveground biomass was expressed in kg dw ha −1.
To compare the plant aboveground biomass of the different cultivated
species (assisted revegetation), the calculation was also made
considering the sum of the plant aboveground biomass in 2 sectors
of each species per plot.
2.4.3. Shoot concentrations of elements in the cultivated species
The concentrations of Cu, N, P, K, Ca, Mg, Zn, Mn, and Fe in the total
aboveground plant material (shoot concentrations) of the cultivated
species were determined after acid digestion and AAS determination
(Sadzawka et al., 2007). To corroborate the precision of the methods, a
certified reference sample of tomato leaves (1573a) from the National
Institute of Standards and Technology was included in the analyses.
The difference between the values obtained in this study and the
certified ones was less than 10%. Spikes were performed on every 10th
sample and recovery was 100% ± 7%.
2.5. Statistical analysis
It was verified that complete random block was an appropriate
design for this experiment. Two-way (amendment type and reveg-
etation regime) variance analysis (ANOVA) for randomized blocks
was used to compare the amendment effects on the soil physico-
chemical characteristics and plant response variables (plant cover,
aboveground biomass, and shoot Cu concentration). In the case of the
assisted revegetation regime, two-way (amendment type and
species) variance analysis (ANOVA) for randomized blocks was used
to compare the plant response variables (plant cover, aboveground
biomass, and shoot Cu concentration). In each case, statistically
significant differences were determined using a Tukey test at p b 0.05.
Simple and multiple regressions were performed between the plant
response variables and soil physicochemical characteristics. Normal
distribution and variance homogeneity of the residuals were verified.
All of the analyses were performed using the programs Excel 2003 and
Minitab 14 (www.minitab.com).
3. Results and discussion
3.1. General characteristics of untreated soil
The topsoil (the top 0–15 cm) of the experimental area is sandy
loam (82% sand, 10% silt and 8% clay). Significant differences among
the blocks of the experimental area were only found for total soil Cu
and OM concentrations (p b 0.05, Table 2). For these variables, the
values were greater in the higher topographical position. Further-
more, total soil Cu and OM concentrations were auto-correlated
(R 2 = 0.80, p b 0.001). This co-occurrence might be explained by the
inhibition of soil heterotrophic microorganisms by metal toxicity
Table 2
Chemical characteristics of topsoils (0–15 cm) in the experimental plots before amendment application.
Topographical position Total Cu Total Zn Total Pb
mg kg−1 mg kg−1 mg kg−1
Low 312 ± 172 a 138 ± 338 a 52 ± 24 ab
Medium 194 ± 71 a 110 ± 22 a 39 ± 7 a
High 607 ± 283 b 149 ± 18 a 76 ± 33 b
Within each block (according to the topographical position), average data and standard deviation (n = 6) are shown. Different letters in the same column indicate significant
differences between the blocks (p b 0.05). OM: organic matter. EC: electrical conductivity determined in saturated paste extract.
⁎ Determined in 0.1 M KNO3 extract at a soil/solution ratio of 1:2.5.
139
(Sauvé, 2006) and by the demonstrated higher deposition of metal-
rich, air-borne particles in the topsoil under the dominant shrubs
where the soil OM concentrations are also higher (Ginocchio et al.,
2004).
Although the experimental area was rather small, the total Cu
concentration in the topsoil varied spatially, ranging between 109 and
920 mg kg −1 (Table 2). In comparison, the total Cu concentration in the
topsoil at Maitencillo (11 km north of the Ventanas industrial complex)
is 60± 1.7 mg kg−1 (Muena et al., 2010). The soils at both sites (Los
Maitenes and Maitencillo) are similar in origin (the parent material is
stabilized paleodunes, Cosio et al., 2007), texture and OM content. As
mentioned above, the high Cu concentration at Los Maitenes is due to
the atmospheric deposition from the Ventanas industrial complex. The
total topsoil Zn and Pb concentrations (Table 2) were also higher at Los
Maitenes than at the background Maitencillo site (Muena et al., 2010).
The free Cu2+ ion is considered to be the primary bioavailable form
of soil Cu (Thakaly et al., 2006), and Cu2+ activity is often considered to
be the best indicator of Cu phytotoxicity (Oliver et al., 2004; Sauvé et al.,
1998). In the Los Maitenes topsoil, the pCu2+ of 5.2 ± 0.5 was 3 units
lower than in the background Maitencillo topsoil (pCu2+ = 8.0 ± 0.6,
Muena et al., 2010). Sauvé et al. (1998) stated that a pCu2+ value below
6.8 decreases the plant yield by 50% for a variety of crops. Therefore, the
free Cu concentration in the Los Maitenes topsoil can be considered
phytotoxic.
The concentrations of available P, K, Ca, and Mg in the topsoil were
in the medium range according to the Chilean classification for crop
production (Rodríguez, 1992), whereas available N was deficient
(b20 mg kg −1; Ruiz, 2001) (see control treatment in Table 3).
3.2. Effects of amendments on the chemical characteristics of the soil
Five months after the amendment application, the revegetation
regime did not have a statistically significant influence on the
physicochemical properties of the soil. Therefore, the average values
and standard deviations (Table 3) were derived from both revegeta-
tion regimes.
The application of lime + compost (LCO) to the soil significantly
increased the concentrations of available N, P, K, Ca, and Mg, and the
moisture content at field capacity of the amended soil was
significantly higher than of unamended control (Table 3). The effect
of the LCO and L treatments on the exchangeable soil Cu was large
(50% reduction) yet not statistically significant (Table 3). This
probably resulted from the high spatial heterogeneity of the soil in
the study area, as reflected by the relative standard deviation of
≈100% in the control soil.
The L and LCO amendments significantly increased the soil pH and
reduced the Cu 2+ activity compared with the unamended control
(Table 3). This probably resulted from the decrease of the proton
activity (increase of pH) in the soil solution and the increased
adsorption of Cu 2+ to the soil and OM particles (McBride, 1994; Sauvé
et al., 1997). McBride et al. (1997) proposed a model to predict Cu 2+
activity and Cu solubility based on the total Cu and OM contents and
the pH of the soil solution. In this study, however, OM was not a
significant variable (p N 0.05) in controlling the Cu 2+ ion activity
(pCu 2+) in the soils 5 months after application. The multiple linear
OM EC Cuex⁎ pH⁎ pCu2+⁎
% dS m−1 mg kg−1
0.8 ± 0.1 a 0.7 ± 0.1 a 7.7 ± 4.8 a 5.0 ± 0.3 a 5.1 ± 0.6 a
0.8 ± 0.2 a 0.7 ± 0.2 a 11 ± 1.1 a 5.1 ± 0.2 a 5.4 ± 0.3 a
1.5 ± 0.5 b 0.9 ± 0.1 a 9.7 ± 5.4 a 5.3 ± 0.5 a 5.1 ± 0.5 a
140 S. Córdova et al. / Geoderma 166 (2011) 135–144

Table 3 3.4. Effect of amendments on plant productivity

Chemical characteristics of topsoil (0–15 cm) in plots after 5 months of amendment
application.
The revegetation regime did not have a statistically significant
Variable Unit Control Lime Lime + Compost influence on the plant productivity (aboveground biomass and plant
pH⁎ 5.4 ± 0.3 a 7.6 ± 0.1 b 7.5 ± 0.1 b cover). Therefore, the average values and standard deviations
pCu2+⁎ 6.0 ± 0.6 a 9.6 ± 0.3 b 9.8 ± 0.4 b (Table 5) were derived from both regimes.
Cuex⁎ mg kg−1 1.5 ± 1.4 a 0.7 ± 0.1 a 0.7 ± 0.0 a The application of lime did not increase either plant biomass or
OM % 0.9 ± 0.2 a 1.0 ± 0.3 a 4.8 ± 1.1 b
cover compared with the control (Table 5). This is contrary to the
EC dS m−1 0.2 ± 0.0 a 0.6 ± 0.1 b 0.8 ± 0.1 c
FC % w/w 31 ± 3 a 32 ± 2 a 42 ± 4 b results from greenhouse studies reported by Goecke et al. (2011) and
N mg kg−1 3.7 ± 1.2 a 4.5 ± 2.3 a 10.4 ± 4.4 b Muena et al. (2010) who observed positive effects of liming on the
P mg kg−1 24 ± 3 a 24 ± 5 a 137 ± 31 b biomass of L. perenne and Oenothera affinis, respectively, grown in Los
K cmolc kg−1 0.3 ± 0.1 a 0.3 ± 0.1 a 1.4 ± 0.1 b Maitenes soil. A source for the discrepancy might be that lime was
Ca cmolc kg−1 6.2 ± 1.0 a 14.9 ± 2.5 b 22.7 ± 4.3 c
more effective in the more contaminated soils used for the
Mg cmolc kg−1 0.9 ± 0.2 a 1.1 ± 0.3 a 2.4 ± 0.5 b
greenhouse studies. The soils used in the greenhouse studies (Goecke
Average data and standard deviation (n = 6) are shown. Different letters in the same
et al., 2011; Muena et al., 2010) had higher total Cu concentrations
row indicate significant differences between the amendments (p b 0.05). OM: organic
matter, FC = field capacity. EC: electrical conductivity determined in saturated paste (655 ± 29 mg kg −1 and 800 ± 11 mg kg −1, respectively), lower pH
extract. (~4.6), lower pCu 2+ (~4.8) and twice as much OM compared with the
⁎ Determined in 0.1 M KNO3 extract at a soil/solution ratio of 1:2.5. soil in this field study. In addition, the irrigation in the greenhouse
study was frequent, and the soil moisture availability was higher than
in this field study.
regression revealed a significant (p b 0.05) influence of total Cu (CuT) The LCO treatment resulted in significant increases in plant
and pH as follows: pCu 2+ = −1.8–1.7 log CuT + 1.8 pH (R 2 = 0.97, productivity when compared with the control (Table 5). The plant
p b 0.001). This relationship confirms our previous finding that soil pH cover following the LCO application was over 80% compared with
was the major factor controlling the free Cu 2+ activity in the soil approximately 50% in the control plots. Similarly, the aboveground
solution in the Los Maitenes area (Neaman et al., 2009). biomass of the spontaneous species following the LCO application
increased by up to 5 times compared with the control. Madejon et al.
3.3. Comparison of plant productivity under the assisted and (2006) observed similar trends in studies of the rehabilitation of Cu-
spontaneous revegetation regimes contaminated soils. The plant cover increased from ~30% to ~ 80% and
the aboveground biomass of the spontaneous species increased from
The amendment type did not have a statistically significant influence 800 kg ha −1 up to 4000 kg ha −1 following compost addition.
on the plant productivity (aboveground biomass and plant cover). A significant interaction was found among the amendment type
Therefore, the average values and standard deviations (Table 4) were and cultivated species, i.e., the different amendments varied in their
derived from all amendment types. effect on the productivity of the different plant species. The best
No statistically significant differences were found in plant pro- combination of species and amendments was C. coronarium/L. perenne
ductivity between the assisted and spontaneous revegetation regimes and LCO with respect to plant cover (Table 6) and C. coronarium and
(p N 0.05). Likewise, under the assisted revegetation regime, the lime + compost with respect to aboveground biomass (Table 7).
aboveground biomass and plant cover of all of the spontaneous species Similar increases in biomass production following the application of
(Appendix 1) were significantly higher than those of all of the cultivated compost to Cu-polluted soils were reported for L. perenne (Goecke
species (Table 4). et al., 2011), corn (De Coninck and Karam, 2008) and Festuca rubra
The reported rates of seeding in metal-polluted soils for phytore- (Simon, 2005). No significant differences with respect to plant pro-
mediation range from 2 to 12 g m −2 (i.e., Bleeker et al., 2002; Bradshaw ductivity were observed for other combinations of cultivated species
and Chadwick, 1980; Department of the Environment, Minerals and amendments (Tables 6 and 7).
Division, 1994; Lautenbech et al., 1995; Mench et al., 2003), whereas Ginocchio (1997) reported the distribution of plant species along a
vegetative transplantation for grasses was of small clumps of 3 to 4 gradient from 4.0 km to 5.5 km south-southeast from the Ventanas
ramets, at a distance approximately 30 cm (Bradshaw and Chadwick, industrial complex. The sampling site 5.5 km from the industrial
1980). In Madejón et al. (2003), 6 sunflower plants per m −2 were used. complex was considered to be relatively unaffected. C. coronarium was
Therefore, our seeding rate (Table 1) is within the range recommended present 5.5 km from the industrial complex, but was absent at the
for the phytostabilization of metal-polluted soils although the planting sampling sites closer to the industrial complex. Therefore, this species
rate is lower. We assume that higher planting/sowing rates than the can be considered to be sensitive to the atmospheric emissions from
ones used in this study would have resulted in rather significant the Ventanas industrial complex. In contrast, O. picensis, M. hastulata,
differences in plant productivity (biomass and cover) under assisted and R. acetosella were present at the sampling sites closer to the
revegetation (Bradshaw and Johnson, 1992). However, at this stage we industrial complex (Ginocchio, 1997), and thus can be considered as
are unable to determine whether assisted revegetation should be more tolerant to atmospheric emissions from the Ventanas industrial
recommended for rehabilitation of this or similar metal-polluted soils. complex.

Table 4 Table 5
Plant cover and aboveground biomass of cultivated and the accompanying spontaneous Plant cover and aboveground biomass 7 months after amendment application.
species under assisted revegetation regime, 7 months after amendment application.
Amendment Plant cover (%) Aboveground biomass
Plant species type Plant cover (%) Aboveground biomass (kg ha−1, dry weight basis)
(kg ha−1, dry weight basis)
Control 53 ± 13 a 709 ± 333 a
Cultivated 9±8 a 246 ± 369 a Lime 55 ± 13 a 886 ± 466 a
Accompanying spontaneous 55 ± 17 b 1387 ± 1083 b Lime + compost 84 ± 6 b 3852 ± 2458 b

Average data and standard deviation (n = 6) are shown. Different small letters in the Average data and standard deviation (n = 6) are shown. Different small letters in the
same column indicate significant differences between the species type (p b 0.05). same column indicate significant differences between the amendments (p b 0.05).
 S. Córdova et al. / Geoderma 166 (2011) 135–144 141

Table 6 Table 8
Plant cover (%) of cultivated plant species in the plots under assisted revegetation. Regressions between plant cover/aboveground biomass and OM content in the soils,
5 months after amendment application (n = 9). For assisted revegetation, the data
Cultivated species Control Lime Lime + compost shown is for all species (cultivated + spontaneous), the total cultivated plant species
C. coronarium 5±3 a 7±5 a 61 ± 23 c and the total accompanying spontaneous plant species.
L. perenne 11 ± 1 a 13 ± 9 a 52 ± 39 bc
Influence of OM content in Plant cover (%) Aboveground
M. hastulata 0±0 a 1±1 a 1±1 a
the soil on: biomass
O. picensis 3±3 a 5±5 a 17 ± 16 ab
(kg ha−1)
R. acetosella 1±1 a 3±2 a 8 ± 10 a
S. chilensis 1±1 a 0±0 a 1±1 a R2 p R2 p

Average data and standard deviation (n = 3) are shown. Different letters indicate Assisted revegetation (total) 0.60 b0.01 0.91 b0.01
significant differences between combinations of species and amendments (p b 0.05). ∑ cultivated 0.70 b0.01 0.84 b0.01
∑ spontaneous – 0.81 b0.01
Spontaneous revegetation 0.79 b0.01 –

In our study, the significant increase in the plant productivity of

C. coronarium with the application of lime + compost (Tables 6 and 7) their root systems were more vigorous and thus their uptake of
suggests that the aided phytostabilization process was successful. The nutrients was more intense.
absence of an increase in the case of O. picensis, M. hastulata, and
R. acetosella can be explained by their higher tolerance to the con- 3.6. Shoot Cu concentrations of cultivated species
taminant exposure and growth conditions, even in unamended soil.
There was a significant interaction between the plant species and
3.5. Identification of variables that affect plant productivity the amendment type for the shoot Cu concentration. The shoot Cu
concentration was similar among most combinations of species
Regression analyses revealed that plant productivity (in terms of and amendments (Figure 4). The only exception was R. acetosella,
either aboveground biomass or plant cover) significantly and posi- (i) which exhibited the highest shoot Cu concentration (686 ±
tively responded to the soil OM content (Table 8). Under the assisted 266 mg kg −1 dw) in the plants of the untreated control and (ii) for
revegetation regime, the soil OM content accounted for 91% and 60% which the application of LCO significantly reduced the shoot Cu
of the variance in aboveground biomass and plant cover, respectively. concentration to that found in all of the other species. Five months
Under spontaneous revegetation, the OM similarly affected plant after the application of the amendments, the pCu 2+ in the topsoil of
cover (R 2 = 0.79, p b 0.01); however, its effect on aboveground the L and LCO treatments was ca. 4 orders of magnitude lower than in
biomass was not statistically significant (Table 8). Other soil chemical the unamended control. Thus, for all of the species with the exception
properties, including the total concentration of Cu, pCu 2+, exchange- of R. acetosella, the Cu accumulation in the aboveground tissues was
able Cu and pH, did not significantly correlate (p ≥ 0.05) with the independent of the Cu availability in the soils.
plant response variables evaluated for both assisted and spontaneous The response of R. acetosella to the Cu concentrations in soils, with
revegetation. increased Cu concentrations in the aboveground tissues, suggests that
The soil OM can improve metal-polluted soils directly by im- it would be considered to be an indicator plant according to the
mobilizing metals, and thus decreasing phytotoxicity, and indirectly classification of Baker (1981). The other species that were not
by improving nutrient availability, soil structure, aeration and water responsive to the soil Cu concentrations would be classified as
retention (Tordoff et al., 2000). Goecke et al. (2011) showed that the excluders, with constant Cu concentrations in the aboveground
positive effect of compost on the productivity of L. perenne grown in tissues. However, to confirm these types of responses, the Cu
pots with the Cu-polluted soil of Los Maitenes was due to improved concentrations in the underground tissues should have been
soil water retention and potassium availability. In accordance with the determined. In Europe, R. acetosella has been described as a pseudo-
latter study, our regression analyses revealed that the vegetation metallophyte species, a plant species with populations that have been
productivity (in terms of either aboveground biomass or plant cover) selected for moderate metal tolerance (Baker et al., 2010).
significantly and positively responded to the soil nutrient availability
and soil water retention capacity (Table 9). Likewise, in some Table 9
cultivated species (Table 10), aboveground biomass was positively Regressions between plant cover/shoot biomass and soil nutrient availability/field
correlated with the foliar concentration of potassium (L. perenne, capacity, 5 months after amendment application (n = 9). For assisted revegetation, the
R 2 = 0.91, p b 0.01, and R. acetosella, R 2 = 0.48, p b 0.05), nitrogen data shown is for all plant species (cultivated + spontaneous), the total cultivated
species and the total accompanying spontaneous species.
(C. coronarium, R 2 = 0.54, p b 0.05), phosphorus (L. perenne, R 2 = 0.53,
p b 0.05), and manganese (M. hastulata, R 2 = 0.76, p b 0.01). Also, the Influence of soil nutrient Plant cover (%) Aboveground biomass
plant cover of C. coronarium was positively correlated with the foliar N availability and the soil field (kg ha−1)
capacity on:
concentration (R 2 = 0.64, p b 0.01). These results suggest that the Variable R2 P Variable R2 P
cultivated species performed better under the LCO treatment because Assisted revegetation (total) P 0.49 b0.05 P 0.64 b0.05
K 0.56 b0.05 K 0.72 b0.01
– – Mg 0.52 b0.05
Table 7 FC 0.54 b0.05 FC 0.55 b0.05
Aboveground biomass (kg ha−1, dry weight) of cultivated plant species in the plots ∑ cultivated K 0.64 b0.05 K 0.59 b0.05
under assisted revegetation. ∑ spontaneous – – P 0.68 b0.01
– – K 0.67 b0.01
Cultivated species Control Lime Lime + compost
– – Mg 0.58 b0.05
C. coronarium 59 ± 31 a 45 ± 26 a 2764 ± 2528 b – – FC 0.60 b0.05
L. perenne 63 ± 59 a 58 ± 18 a 331 ± 79 a Spontaneous revegetation N 0.68 b0.01 N 0.46 b0.05
M. hastulata 3±3 a 4±5 a 31 ± 39 a P 0.81 b0.01 P 0.52 b0.05
O. picensis 25 ± 29 a 20 ± 26 a 576 ± 624 a K 0.81 b0.01 K 0.54 b0.05
R. acetosella 20 ± 6 a 25 ± 19 a 184 ± 239 a Ca 0.79 b0.01 Ca 0.48 b0.05
S. chilensis 2±2 a 2±1 a 2±2 a Mg 0.88 b0.01 – –
FC 0.78 b0.01 FC 0.62 b0.05
Average data and standard deviation (n = 3) are shown. Different letters indicate
significant differences between combinations of species and amendments (p b 0.05). FC: field capacity.
142 S. Córdova et al. / Geoderma 166 (2011) 135–144

Table 10
Shoot element concentrations of macro- and micronutrients in the cultivated species, 7 months after amendment application.

Amendment Species N P K Ca Mg Zn Mn Fe
% % % % % mg kg−1 mg kg−1 mg kg−1

Control C. coronarium 0.5 ± 0.1 0.3 ± 0.1 0.6 ± 0.3 1.8 ± 0.6 0.2 ± 0.1 79 ± 16 35 ± 16 206 ± 45
Lime C. coronarium 0.5 ± 0.1 0.3 ± 0.0 1.2 ± 0.3 1.5 ± 0.1 0.2 ± 0.0 101 ± 36 34 ± 19 176 ± 50
Lime + compost C. coronarium 0.8 ± 0.3 0.3 ± 0.1 1.2 ± 0.4 1.4 ± 0.6 0.3 ± 0.1 60 ± 31 48 ± 15 161 ± 62
Control L. perenne 0.8⁎ 0.2 ± 0.0 0.9 ± 0.1 0.7 ± 0.1 0.2 ± 0.0 80 ± 11 116 ± 30 453 ± 117
Lime L. perenne 0.9 ± 0.1 0.1 ± 0.0 1.0 ± 0.2 1.1 ± 0.4 0.3 ± 0.1 52 ± 15 71 ± 16 261 ± 33
Lime + compost L. perenne 1.2 ± 0.2 0.2 ± 0.0 2.0 ± 0.4 0.6 ± 0.1 0.2 ± 0.0 42 ± 2 129 ± 57 221 ± 40
Control M. hastulata n.d. 0.1 ± 0.1 0.7 ± 0.2 0.8 ± 0.4 0.2 ± 0.1 52 ± 19 21 ± 10 230 ± 102
Lime M. hastulata n.d. 0.2 ± 0.1 1.0 ± 0.5 0.9 ± 0.4 0.1 ± 0.0 53 ± 20 25 ± 4 475 ± 290
Lime + compost M. hastulata n.d. 0.3 ± 0.2 1.2 ± 0.5 0.8 ± 0.1 0.2 ± 0.1 51 ± 15 35 ± 27 172 ± 48
Control O. picensis 0.8⁎ 0.2 ± 0.1 1.2 ± 0.3 2.0 ± 0.8 0.3 ± 0.2 65 ± 22 86 ± 5 263 ± 30
Lime O. picensis 0.6⁎ 0.2 ± 0.1 1.2 ± 0.3 2.1 ± 1.3 0.2 ± 0.1 39 ± 3 52 ± 5 125 ± 47
Lime + compost O. picensis 0.7 ± 0.3 0.2 ± 0.0 1.1 ± 0.1 2.2 ± 0.9 0.2 ± 0.0 31 ± 8 43 ± 12 145 ± 33
Control R. acetosella 0.6 ± 0.1 0.1 ± 0.0 0.3 ± 0.1 0.7 ± 0.0 0.1 ± 0.0 210 ± 30 104 ± 13 1538 ± 340
Lime R. acetosella 0.7⁎ 0.2 ± 0.1 0.4 ± 0.2 0.8 ± 0.3 0.2 ± 0.1 107 ± 32 51 ± 10 525 ± 112
Lime + compost R. acetosella 0.9 ± 0.1 0.1 ± 0.1 0.3 ± 0.6 0.6 ± 0.3 0.2 ± 0.0 68 ± 23 100 ± 20 861 ± 1033
Control S. chilensis n.d. 0.2 ± 0.1 1.3 ± 1.0 1.8 ± 0.3 0.3 ± 0.2 220 ± 34 74 ± 48 582 ± 152
Lime S. chilensis n.d. 0.2 ± 0.1 2.8 ± 0.7 1.6 ± 0.8 0.3 ± 0.1 43 ± 15 17 ± 8 320 ± 62
Lime + compost S. chilensis n.d. 0.3 ± 0.2 3.1 ± 1.0 1.9 ± 1.1 0.4 ± 0.2 40 ± 31 20⁎ 191 ± 194

Average data and standard deviations (n = 3) are indicated. n.d.: not determined due to small biomass available.
⁎ Average of duplicate.

The findings of this study are in agreement with those of Ginocchio
(1997) who reported the shoot Cu concentrations of the plant species
5.5 km from the Ventanas industrial complex, where the total Cu
concentration in the soil is 172 mg kg −1 (Ginocchio et al., 2006). At
that site, the shoot Cu concentrations of C. coronarium, R. acetosella, O.
picensis, and M. hastulata were 170 mg kg −1 , 130 mg kg −1 ,
210 mg kg −1, and 145 mg kg −1, respectively. Although the total soil
Cu concentration in the soils of our study are considerably higher
(Table 2) than those of the site in Ginocchio (1997), the shoot Cu
concentrations of C. coronarium, R. acetosella, O. picensis, and M.
hastulata are similar (Figure 4). These results suggest that Cu
accumulation in the aboveground tissues of these plant species was
independent of the Cu availability in the soils.
It should be considered that most of the plant species considered in
this study have trichomes or glands on their leaves, retaining soil
particles on their external surfaces. This might make it difficult to
completely eliminate external tissue contamination even after
the washing protocol used. Although the washing procedure used
in this study was thorough, the possibility exists that persistent
external contamination of the aerial plant tissues were not completely
removed.
4. Conclusions
The application of lime and lime + compost decreased the Cu 2+
activity in the soil solution, showing effective immobilization of this
element in the soils of the Puchuncaví Valley.
Plant productivity (cover and aboveground biomass) was the same
under the assisted and spontaneous revegetation regimes for the
planting/sowing rates used in this study, suggesting that plant
cultivation is unnecessary. The native soil seed bank was sufficient
for attainment of the proper plant cover and biomass production after
the application of soil amendments.
The application of lime had no effect on plant productivity in
comparison with the control, whereas the application of lime +
compost was effective in increasing the plant cover and aboveground
biomass. Simple and multiple regressions showed that this effect
was mainly due to the increased OM content and not to the increase in
soil pH.
Although the pCu 2+ in the amended soils was 4 orders of
magnitude higher than in the unamended control, the shoot Cu
concentration was similar among most combinations of plant species
and amendments. These results suggest that the Cu accumulation in

1000
Control Lime Lime + compost
bc
Cu concentration (mg kg-1)

800 c

600 ab

400
a
ab a
a a a a a a
200 a a a
a a
a

0
C. coronarium L. perenne M. hastulata O. picensis R. acetosella S. chilensis
Cultivated species

Fig. 4. Shoot Cu concentration in cultivated plant species. Average data and standard deviation (n = 3) are shown. Different letters indicate significant differences between
combinations of plant species and amendments (p b 0.05).
 S. Córdova et al. / Geoderma 166 (2011) 135–144 143

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