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International Journal of
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Metal Uptake by Native Plants and

Revegetation Potential of Mining Sulfide-
Rich Waste-Dumps
a c b a
Patrícia Gomes , Teresa Valente , Jorge Pamplona , Maria
a b c
Amália Sequeira Braga , José Pissarra , José António Grande Gil
c
& Maria Luisa de la Torre
a
Centro de Investigação Geológica, Ordenamento e Valorização
de Recursos (CIG-R) , Universidade do Minho , Campus de Gualtar,
Braga , Portugal
b
Click for updates Departamento de Biologia, Faculdade de Ciências , Universidade
do Porto , Rua Campo Alegre s/n, Porto , Portugal
c
Centro de Investigación para la Ingeniería en Minería Sostenible
(CIPIMS), Escuela Técnica Superior de Ingeniería , Universidad de
Huelva , Ctra. Palos de la Frontera, s/n., Palos de la Frontera,
Huelva , Spain
Accepted author version posted online: 17 Jul 2013.Published
online: 25 Feb 2014.

To cite this article: Patrícia Gomes , Teresa Valente , Jorge Pamplona , Maria Amália Sequeira Braga ,
José Pissarra , José António Grande Gil & Maria Luisa de la Torre (2014) Metal Uptake by Native
Plants and Revegetation Potential of Mining Sulfide-Rich Waste-Dumps, International Journal of
Phytoremediation, 16:11, 1087-1103, DOI: 10.1080/15226514.2013.810586

To link to this article: http://dx.doi.org/10.1080/15226514.2013.810586

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 International Journal of Phytoremediation, 16:1087–1103, 2014
Copyright C Taylor & Francis Group, LLC

ISSN: 1522-6514 print / 1549-7879 online

DOI: 10.1080/15226514.2013.810586

METAL UPTAKE BY NATIVE PLANTS

AND REVEGETATION POTENTIAL OF MINING
SULFIDE-RICH WASTE-DUMPS
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Patrı́cia Gomes,1 Teresa Valente,1,3 Jorge Pamplona,1

Maria Amália Sequeira Braga,1 José Pissarra,2
José António Grande Gil,3 and Maria Luisa de la Torre3
1
Centro de Investigação Geológica, Ordenamento e Valorização de Recursos
(CIG-R), Universidade do Minho, Campus de Gualtar, Braga, Portugal
2
Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua
Campo Alegre s/n, Porto, Portugal
3
Centro de Investigación para la Ingenierı́a en Minerı́a Sostenible (CIPIMS),
Escuela Técnica Superior de Ingenierı́a, Universidad de Huelva. Ctra. Palos de la
Frontera, s/n., Palos de la Frontera, Huelva, Spain

Waste dumps resulting from metal exploitation create serious environmental damage, pro-
viding soil and water degradation over long distances. Phytostabilization can be used to
remediate these mining sites. The present study aims to evaluate the behavior of selected
plant species (Erica arborea, Ulex europaeus, Agrostis delicatula, and Cytisus multiflorus)
that grow spontaneously in three sulfide-rich waste-dumps (Lapa Grande, Cerdeirinha, and
Penedono, Portugal). These sites represent different geological, climatic and floristic settings.
The results indicate distinctive levels and types of metal contamination: Penedono presents
highest sulfate and metal contents, especially As, with low levels of Fe. In contrast, at Lapa
Grande and Cerdeirinha Fe, Mn, and Zn are the dominant metals. In accordance, each
waste dump develops a typical plant community, providing a specific vegetation inventory.
At Penedono, Agrostis delicatula accumulates As, Pb, Cu, Mn, and Zn, showing higher
bioaccumulation factors (BF) for Mn (32.1) and As (24.4). At Cerdeirinha, Ulex europaeus
has the highest BF for Pb (984), while at Lapa Grande, Erica arborea presents high BF
for Mn (9.8) and Pb (8.1). Regarding TF, low values were obtained for most of the metals,
especially As (TF < 1). Therefore, the results obtained from representative plant species
suggest appropriate behavior for phytostabilization measures.

KEY WORDS: phytostabilization, metalliferous wastes, bioaccumulation factor, translocation factor, Portugal

INTRODUCTION
The mining industry has produced a significant environmental degradation legacy.
The most serious environmental and landscape damage is represented by abandoned waste

Address correspondence to Teresa Valente, Centro de Investigação Geológica, Ordenamento e Valorização

de Recursos (CIG-R), Departmento de Ciências da Terra, Universidade do Minho, Campus de Gualtar, 4710-057
Braga, Portugal. E-mail: teresav@dct.uminho.pt
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bijp.

1087
 1088 P. GOMES ET AL.

dumps that contain reactive wastes, such as sulfide-rich materials. Sulfide minerals are
susceptible to weathering, mobilizing metals, sulfate, and acidity through acid mine
drainage (AMD) processes (e.g., Valente and Leal Gomes, 2009 a, b; Grande et al. 2010).
In metalliferous mines with sulfide-rich paragenesis, AMD is often responsible for toxic
effects and metal dispersion to surrounding ecosystems (Valente et al. 2011 a, b).
Natural revegetation is a relevant process for mining ecosystem recovery. However,
in the presence of very reactive wastes, technical intervention is often necessary. In this
scenario, environmentally friendly approaches (Bradshaw 1998; Tordoff et al. 2000; Wong
2003), such as phytoremediation, emerge as a competitive technology for waste-dump
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restoration and management (Sas-Nowosielska et al. 2004; Wenzel 2009; Salt et al. 1998;
McGrath et al. 2002; Samardjieva et al. 2011).
The economic viability and ecological sustainability of phytostabilization (Miller
1996) separate it from other phytoremediation techniques (Schnoor 1997; Chaney et al.
1997; McGrath and Zhao 2003). Absorption and immobilization of metals through plants,
which involves phytostabilization, reduces metal mobility and dispersion by water or air.
It contributes to the physical stabilization of waste dumps, minimizing erosion and the
effects of wind and water dispersion (Abreu et al. 2008; Susarla et al. 2002). How-
ever, general properties of sulfide-rich wastes restrict the establishment of dense plant
communities. These features, together with the chemical properties of waste, constrain
revegetation processes in several ways. Some constraints come from inappropriate phys-
ical properties, poor organic matter and nutrient supply. Others are related to acidity
and high metal levels, which induce toxicological effects. In general, plants can absorb
significant amounts of metals through root uptake and foliar absorption (Forstner and
Wittmann 1981). However, a total metal concentration >0.1% is generally considered
to be toxic to plants (Williamson and Johnson 1981). Additionally, interactions occur-
ring in soil-plant systems are complex and the availability of metals in plants varies
considerably, depending on many factors, namely soil pH and redox potential, organic
matter, cation exchange capacity, mineralogy, texture and structure (Albasel and Cottenie
1985).
Phytostabilization of many small to medium sized waste dumps is promoted by natural
revegetation. The success of this natural process depends on plant colonization with certain
characteristics, such as good absorption capacity, deep root system, accelerated growth
rate and resistance to pollutants (Valente et al. 2012a). Indeed, plants that grow naturally
in an area are better suited for survival, growth and reproduction under environmental
stresses than plants coming from other environments (Del Rio et al. 2002; Nazir et al.
2011). Therefore, native plants are most appropriate for phytostabilization, providing certain
benefits, such as wildlife habitat.
This study focuses on the role played by native plants in sulfide-rich waste-dump
restoration. Three distinct mines located in the north of Portugal were presented as mod-
els of geological, mineralogical, climatic and floristic diversity. The following aims were
defined: i) undertake an inventory of native plants and detailed description of the adapted
plant communities; ii) evaluate the influence of selected soil properties on revegetation
success; iii) an evaluation of the ability of selected species (Erica arborea, Ulex europaeus,
Agrostis delicatula, and Cytisus multiflorus) to accumulate and translocate As, Pb, Cu,
Mn, Zn, and Bi in the respective geochemical environments; iv) assess the phytostabi-
lization potential of dominant species for application in similar geological and climatic
conditions.
 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1089

METHODS
Description of Study Areas
The three sites under study, Lapa Grande, Cerdeirinha, and Penedono, are represented
in Figure 1. Lapa Grande and Cerdeirinha are located in northern Portugal, in a region where
metal mining has a large and long tradition. Both sites were affected by the exploitation
of tungsten minerals (W) in a skarn ore deposit with abundant sulfides (mainly pyrrhotite
and pyrite) (Coelho 1993; Valente 2004). The mining activities, which took place until the
1980s, resulted in enriched sulfide waste dumps. Although similar, the two waste dumps
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differ in terms of the ratio of sulfide to minerals with neutralizing potential (calcite, apatite,
and Ca and Al-silicates), which is higher in Cerdeirinha (Valente 2004; Valente et al.
2012a).
The third site, Penedono mine, is located in northeastern Portugal and results from
the exploitation of sulfide-rich gold quartz veins, associated to second order shear zones
(Silva and Neiva 1990; Sousa and Ramos 1991; Leal Gomes and Castelo Branco 2003).
In similarity with the other two sites, waste dumps at Penedono are mainly composed of
fine sand grain size tails resulting from milling, hydrogravitic separation and flotation.
However, the paragenetic scenario from Penedono’s ore deposit is different and, therefore,
the waste dumps have different geochemical and mineralogical behaviors. The inherited

Figure 1 Location of the three study areas and definition of the respective sampling sites.
 1090 P. GOMES ET AL.

mineralogy which characterizes Penedono’s mine wastes is rather monotone, with high
arsenopyrite proportion, Al-silicates and significant absence of neutralizing minerals. On
the contrary, the skarn rocks from Lapa Grande and Cerdeirinha contributed to a more
diversified mineralogy, liberating minerals with both acidifying and neutralizing potential
Around Lapa Grande and Cerdeirinha, the landscape presents typical shrubland fea-
tures, strongly affected by frequent seasonal fires. The plant community is dominated by
Ulex europaeus, Ulex minor, Cytisus striatus, Erica arborea, and Pterospartum tridenta-
tum. On the flattened areas there are small tree woods, dominated by Betula alba, Pinus
pinaster and Quercus sp.
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In Penedono, the landscape is marked by an open valley (oriented N-S) and by small
agricultural plots and pasture lands. At higher elevations, vegetation is sparse and dominated
by shrubs, such as Cytisus multiflorus, Cytisus striatus, and Erica lusitanica. The arboreal
stratum is dominated by Castanea sativa, Pinus pinaster, and Quercus pyrenaica.

Soil and Plant Sampling

Sampling took place between February and June 2011, according to the location of
the sampling stations shown in Figure 1. The sampling sites were established in order to
represent conditions of topographic, microclimatic and floristic diversity. Their location
was also affected by some areas with difficult access due to steep slopes and strong erosion,
especially affecting Lapa Grande and Penedono. Waste-dump material was collected at
each site (6 to 8 samples). Samples were collected using a stainless steel auger with 17 cm
height. The first 5 cm of top soil containing organic matter and vegetation were scraped and
rejected. At each sampling site, a pooled sample was obtained from a circular area of 50 cm
(3 sub-samples). Soil samples were dried in lab at 40◦ C for 72 h, separated with a 2 mm
grain size sieve, homogenized and pulverized (in an Agate mortar) to <105 μm (Valente
et al., 2011b). A total of 21 soil samples were collected from the three waste dumps.
A total of 12 to 14 plant samples were collected from each waste dump, as represen-
tative species of the waste dump community. Plant species (Table 1) were chosen for their
abundance in the respective locations, good vegetative growth and being the first plants to
colonize the respective waste dump. For each plant, shoots and roots were separated prior
to further treatment. Table 1 presents a list of plant samples (roots and shoots) obtained in
each waste dump. Plants were carefully washed with abundant distilled water, rinsed with
ultra-pure water and then dried at 50◦ C for 72 h (Gomes 2011). Additionally, three sam-
ples of rhizospheric soil were collected from each site: Lapa Grande from Erica arborea,
Cerdeirinha from Ulex europaeus, and Penedono from Agrostis delicatula.

Table 1 List of plant samples (S – Shoots; R – Roots).

Waste-dump Species Plant samples

Lapa Grande Erica arborea LG1-S; LG1-R; LG2-S; LG2-R; LG3-S; LG3-R; LG4-S;
LG4-R; LG5-S; LG5-R; LG6.1-S; LG6.1-R; LG6.2-S;
LG6.2-R
Cerdeirinha Ulex europaeus C1-S; C1-R; C2-S; C2-R; C3-S; C3-R; C4-S; C4-R; C5-S;
C5-R; C6-S; C6-R
Penedono Agrostis delicatula P1-S; P1-R; P2-R; P2-S; P3-S; P3-R; P5-S; P5-R; P6-S; P6-R;
P8-S; P8-R
Cytisus multiflorus
 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1091

Analytical Methods
The soil’s organic matter (OM) was estimated by loss on ignition method (Wilke
2005). Electrical conductivity (EC) and pH were measured in a soil slurry solution 1:2.5
ratio (m/v) with a multiparameter meter (Orion, model Star 5). Soil pH was also determined
in KCl solution, 1M (Wilke 2005). Sulphate (SO4 2−-S) and water-extractable nutrients,
ammonium (NH4+-N), phosphate (PO4 −3-P), and nitrate (NO3 −-N), were obtained in a 1:5
soil: water extract, following the procedure described by Marion et al. (1991) and Pino et al.
(2008). Ammonium-nitrogen was analyzed by potentiometry, using an Orion Probe, ref.
951201, while the other ions were determined by ion chromatography (IC) with suppressed
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conductivity detection (761 Compact IC Metrohm). Soil metal and metalloid concentrations
(Fe, Pb, As, Cu, Mn, Zn, and Bi) were obtained by inductively coupled plasma-mass
spectrometry (ICP/MS) after an Aqua Regia extraction. The vegetation analyses were
performed by ICP/MS after digesting with HNO3 and H2 O2 . These analyses were performed
at Activation Laboratory, Ltd (Actlabs, Canada), including duplicate samples and precision
blank checks, whereas accuracy was obtained by using certified standards (GXR series).
Granulometric and mineralogical analyses. Quantitative assessment of per-
centage for different grain sizes in the coarser fractions was performed by screening, using
a standard series of sieves between 0.062 and 2 mm. Silt- and clay-sized material classifi-
cation was obtained using the automated SediGraph. The texture classification was based
on the USDA soil texture diagram.
The mineralogy of the soil was analyzed by x-ray powder diffraction (XRD) with
a Philips X’pert Pro-MPD diffractometer, using Cu-Kα radiation, operated with a 2 theta
step size of 0.02◦ and a counting time of 1.25s. The XRD diffractograms were obtained
from powders (bulk sample <2 mm) and from oriented aggregates (<2 μm fraction).
A semi-quantitative analysis was performed by using the peak-height intensities of the
diagnostic reflections (Valente et al. 2012b). Morphological and compositional aspects of
the rhizospheric soil were analyzed by SEM (on carbon coated samples) with a LEICA
S360 microscope, combined with an energy dispersive system (SEM-EDS).

Statistical Analysis
The experimental data were subject to the analysis of variance (ANOVA), using
the Statgraphic Centurion package. The Tukey test was applied to detect the statistical
significance of the differences (P < 0.05) between the obtained averages. The method
used to discriminate among the averages (Multirange test) was Fisher’s least significant
difference (LSD) procedure.

RESULTS AND DISCUSSION

Textural and Mineralogical Characterization
The particle size analysis indicates sand- and silt-sized fractions as prevalent. The
“clay” class content (<2 μm) is low in the three cases (∼1%). Therefore, in terms of
texture, soil samples exhibit coarse textures. Besides texture, clay fraction composition is
of major importance for controlling the substrate’s ability to support vegetation. Although
comparable in texture, different clay mineralogy was revealed on a previous study (Gomes
2011). Figure 2 presents the mineralogical composition of the <2 μm fraction. Among clay
 1092 P. GOMES ET AL.
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Figure 2 Mineralogical composition of <2 μm fraction.

minerals, kaolinite is abundant. Additionally, the hydroxysulfate jarosite was abundantly

detected at the three sites.
The morphology study by SEM indicates that the kaolinite group is represented by the
halloysite, identified by its tubular shape (Fig. 3a). No significant differences were found
between bulk soil and rhizospheric soil, concerning clay mineralogy. Nevertheless, in the
rhizosphere area is common to observe the retention of primary and secondary minerals,

Figure 3 SEM – EDS images obtained in rhizospheric soil from Cerdeirinha. A) Spherical aggregates of tubular
halloysite. B) Botryoidal aggregates of calcite precipitated in the plant roots.
 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1093

including the ore minerals scheelite and wolframite. Additionally, Figure 3b shows a net of
botryoidal calcite that precipitates on the roots of Ulex europaeus.
A major difference between the sites lies on the diversity of minerals that compose
the <2 μm fraction. At Penedono, kaolinite is the most abundant phase (40%). On the
other hand, the other two sites (Lapa Grande and Cerdeirinha) show higher mineralogical
variety (chlorite, vermiculite, smectite, and mixed-layered minerals). This is in agreement
with the lower diversity observed for the ore paragenesis in Penedono.
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Soil Properties and Metal Concentrations

Selected properties for the 21 soil samples are listed in Table 2. Soil analysis showed
that the samples have pH values in the acidic range (<4.5). ANOVA’s P-value (0.0689),
greater than 0.05, confirms that there is statistically no significant difference between the
average values of the three sites, concerning the pH. Rhizosphere is a microbiosphere with
particular properties (Zhongwen 2002; Wenzel 2009) and, although the pH of the bulk soil
is acidic, different plants may have different rhizosphere pH. However, in the present study
no significant differences were detected between bulk soil and rhizospheric soil.
A major difference lies in the organic matter content (OM) of the samples from
Penedono, as demonstrated by the ANOVA multirange test. At this site, the average is very
low (less than 1%), while Cerdeirinha and Lapa Grande have average values close to normal
soils (∼5%). This can be justified by the different vegetal colonization in waste dumps and
surroundings. At Lapa Grande there are big old trees that contribute to form an organic
horizon (horizon O, FAO designation) (FAO 2006), covering almost all the studied area. In
addition, topographic features, such as slope orientation and sun exposure, promote higher
humidity in Lapa Grande. This favors moss colonization and enhances organic matter
values. Plant colonization density is small at Penedono, which is characterized by sparse
and small plants.
The three sites also differ significantly (ANOVA-P < 0.05), regarding water-
extractable ammonium (NH4 +-N) and phosphate (PO4 −3-P). However, the analyzed nu-
trients are present in low concentration, which is typical in mining environments (Wong
2003). In these conditions, the competition for nutrients, such as nitrogen or phosphorus,
represents a limiting factor for plants and soil microorganisms (Unterbrunner et al. 2007).
According to Valente et al. (2011 b), the skarn nature of Cerdeirinha and Lapa Grande’s
ore deposit may lead to a richer mineral reserve for plants, associated to the presence of
minerals that may furnish nutrients (such as apatite).
In the three sites, sulfate is the dominant anion. Although there is no significant
difference (ANOVA-P = 0.4908), Penedono presents the highest average concentration.
This is in accordance with the less diversified ore paragenesis, as pointed by Valente et al.
(2011b).
In terms of metal concentrations (Table 2), results show that Lapa Grande and Cerdeir-
inha have a similar contamination degree for almost all elements. In fact, ANOVA mul-
tirange test indicates that Penedono statistically shows significant differences (at the 95%
confidence level), regarding Fe, As, Pb, Mn, and Zn. Fe and Mn are the most abundant
metals in Lapa Grande and Cerdeirinha. Here, the concentration of Fe is above 10% in
most samples, while in Penedono, its average is considerably lower (1.5%). These results
are consistent with ore deposit paragenesis, which supply iron from iron sulfides in Lapa
Grande and Cerdeirinha (Valente et al. 2012). On the other hand, arsenic and lead averages
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1094
Table 2 Average and range values for typical soil parameters and metals. LG – Lapa Grande; C – Cerdeirinha; P – Penedono.

(mg/kg) (As,Pb,
EC Cu,Mn,
Waste-dumps pH (KCl) (μS/cm) MO (%) N-NO3 − N-NH4 + P-PO4 3− SO4 2− As Pb Cu Mn Zn Bi Fe (%) Zn,Bi)

LG (n = 7) 3.42 111 5.4 0.64 0.83 2.31 298 1,745 15 237 2,842 317 142 11 5,298
(2.82–3.77) (40–409) (4.1–7.3) (0–1.50) (0.15–1.95) (0.10–4.85) (5.5–1,620) (290–7,640) (9–20) (125–406) (971–4,230) (218–378) (46–286) (8–16)
C (n = 6) 3.89 96 5.3 1.42 1.13 0.07 149 2,670 4.5 385 2,250 335 238 12 5,882
(3.39–4.13) (60–193) (4.6–6.3) (0–2.00) (0–2.45) (0–0.20) (70–380) (2,080–3,080) (1–10) (253–724) (1,540–4,310) (243–419) (185–284) (11–13)
P (n = 8) 3.55 112 0.86 0.75 0.12 0.09 410 7,091 66 15 30.5 16 46 1,5 7,265
(3.20–4.33) (11–237) (0.21–1.92) (0–3.50) (0–0.45) (0–0.35) (8–945) (2,330–10,600) (18–195) (4–29) (9–132) (9–28) (25–104) (1–3)
 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1095

are significantly higher in Penedono (7.091 mg/kg for As and 66 mg/kg for Pb). Soil con-
tamination by metals was already registered by Abreu et al. (2007). These authors found
arsenic concentration of 40.000 mg/kg and mentioned eolic and hydric dispersion with As
concentrations as high as 23.900 mg/kg in Penedono’s surrounding soils. On the contrary,
in Lapa Grande and Cerdeirinha the arsenic average levels are less than 3.000 mg/kg.
The effects of toxic metals on plants depend on many factors, including plant species
and soil properties. However, it can be assumed that, generally, the total metal concentration
in the three waste dumps are phytotoxic (>0.1%) (Tordoff et al. 2000; Williamson and
Johnson 1981; Adriano 2001). In summary, Penedono has higher levels of metal contents,
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while Lapa Grande and Cerdeirinha have similar average values.

Plant Community
Table 3 presents an inventory of plant species identified in the studied areas. In
the three sites, there are species known by their tolerance and/or as metal and arsenic
hyperaccumulators (e.g., Koe and Jaques 1993). There are several bibliographic references
in regard to the presence of Cytisus, Agrostis and Erica species in sulfide waste dumps,
in the Iberian Peninsula mining sites (Abreu et al. 2007, 2008; De Koe and Jaques 1993).
The arboreal species, Pinus pinaster and Quercus sp. are typical elements of the northern
Portugal landscape (Pratas et al. 2005; Favas 2008).
The maps in Figure 4 show a specific plant association for each waste dump, as well as
the respective substrate coverage percentage, obtained by vegetation field mapping. Pene-
dono shows the most intense signs of geochemical and mineralogical instability (Valente
et al. 2012) and similarly the highest uncovered area. In a similar way, field observations
indicate that the uncovered or poorly vegetated areas in Lapa Grande and Cerdeirinha match
with the most reactive waste-dump portions.

Soil – plant Relation

Metals in plant biomass. Average concentrations of metals in the roots (R) and
shoots (S) of the analyzed plants are provided in Table 4. The results indicate that the four
selected species are suffering the effects of contamination. The analyzed metals occur in
higher levels than the average ones (background levels) found in plants growing in normal
conditions (Kabata-Pendias 2001). Erica arborea roots show the highest concentration of
Cu (3.267 mg/kg) and Mn (49.314 mg/kg). On the other hand, Ulex europaeus shows the
highest concentrations of Pb and Bi in its biomass (both roots and shoots). Arsenic is the
major contaminant in Agrostis delicatula, with 6.745 mg/kg in the roots and 4.220 mg/kg
in the shoots. In Cytisus multiflorus roots there are As, Mn and Zn with 4.473, 2.205,
and 1.249 mg/kg, respectively. In the shoots of this species, Mn is the dominant metal
(9.683 mg/kg).
Results also show that plants respond differently to high soil metal levels. ANOVA
analysis indicates that although there is statistically no significant difference (at the 95%
confidence level) between Zn and Bi from one species to another, a distinct behavior
is observed for arsenic and other metals. Regarding Mn and Cu, Erica arborea denotes
a significant difference from Agrostis delicatula and Cytisus multiflorus with the same
confidence level. Identically, regarding arsenic, Agrostis delicatula behaves differently
from the other three species.
 1096 P. GOMES ET AL.
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Figure 4 Vegetation maps and relative abundance of most representative species.

 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1097

Table 3 Plant species present in the three waste-dumps.

Family and Species Cerdeirinha Lapa Grande Penedono

Arboreous Betulaceae
Betula alba ∗

Fagaceae
Quercus robur ∗ ∗

Myrtaceae
Eucalipus globulus ∗

Pinaceae
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Pinus pinaster ∗ ∗ ∗

Arbustive Cistaceae
Cistus psilosepalus ∗

Halimium alyssoides ∗

Ericaceae
Erica arborea ∗ ∗

Erica ciliaris ∗

Erica umbellata ∗

Leguminosae
Cytisus multiflorus ∗

Cytisus striatus ∗ ∗

Genista florida ∗ ∗

Ulex europaeus ∗ ∗

Rosaceae
Rubus spp ∗ ∗

Herbaceous Boraginaceae
Lithodora prostrata ∗

Campanulaceae
Jasione montana ∗

Cistaceae
Therocistus guttatus ∗

Compositae
Andryala integrifolia ∗ ∗

Leontondon taraxacoides ∗

Gramineae
Agrostis curtisii ∗ ∗

Agrostis delicatula ∗ ∗

Briza minor ∗

Holcus lanatus ∗ ∗ ∗

Rosaceae
Potentilla erecta ∗

Scrophulariaceae
Verbascum thapsus ∗

Dennstaedtiacea

Bioaccumulation Factor (BF). Metal accumulation in plants is often expressed as

the bioaccumulation factor (BF). It is calculated as the ratio between the metal concentration
in plant shoots and the metal concentration in the soil (Mattina et al. 2003). The BF values
obtained for the studied plants are shown in Figure 5. These results indicate that the four
species are able to accumulate most of the analyzed elements. An important exception was
observed for arsenic on three of them: BF values are less than 1 for Ulex europaeus (0.071),
Erica arborea (0.032), and Cytisus multiflorus (0.704). This could be an advantage in the
case of phytostabilization procedures with less risk of As entering the food chain.
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1098
Table 4 Average and range concentrations of metal in Roots (R). Shoots (S) and Background levels∗ (Kabata-Pendias and Pendias. 2001). LG – Lapa Grande; C – Cerdeirinha;
P – Penedono

(mg/kg)

Waste-dump Plant species Mn Cu Zn As Pb Bi

LG Erica arborea (n = 7) R 49,314 (23,000–73,100) 3,267 (1,200–5,870) 1,190 (259–4,660) 451 (158–766) 49 (7.9–116) 71 (55–107)
S 25,374 (1,020–34,600) 359 (178–502) 811 (492–1,020) 59 (10–266) 138 (24–287) 6 (2–20)
C Ulex europaeus (n = 6) R 911 (101–1,860) 1,824 (61.7–3,660) 894 (94–1,990) 682 (49–1,180) 908 (48.3–1,660) 96 (7.53–194)
S 3,548 (2,750–4,330) 385 (204–712) 902 (732–1,390) 200 (67–440) 2,883 (1,530–4,900) 23 (4.18–65.9)
P Agrostis delicatula (n = 3) R 154 (127–181) 96 (92.1–98.9) 204 (111–297) 6,745 (4,890–8,600) 59 (38.2–80.1) 38 (29.1–46.1)
S 630 (562–698) 51 (37.8–64.4) 196 (185–206) 4,220 (4,030–4,410) 44 (34.4–52.8) 33 (26.6–38.5)
Cytisus multiflorus (n = 3) R 2,205 (745–3,640) 285 (189–381) 1,249 (798–1,660) 4,473 (2,430–6,340) 62 (32.9–109) 28 (18.2–45.8)
S 9,683 (1,490–21,300) 306 (190–482) 1,294 (963–1,740) 2,035 (766–4,290) 44 (13–81) 23 (3.3–59.2)
Background levels in plants∗ 30–300 5–30 25–150 1–1.5 5–10
 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1099
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Figure 5 Bioaccumulation factor (BF) of each species for different elements. Black bars on columns are standard
error (n = 3–7).

It should be highlighted the high value observed for Pb (984) in Ulex europaeus.
Regarding Agrostis delicatula, this was the only plant able to accumulate all the analyzed
elements, in particular Mn, Zn, and Cu.
These analyses show that not all chemical elements were retained in the same way in
the plant, suggesting that tolerance to a particular element does not necessarily guarantee
tolerance to others (Antosiewicz 1992; González and González-Chávez 2006).
Translocation Factor (TF). The translocation factor (TF) (Figure 6) represents
the ratio between metal concentration in shoots and roots, according to equation 1
(Matina et al. 2003), and defines the plant’s effectiveness to translocate metals to the
shoots.

TF = [Shoots]/[Roots] (1)

Regulation of metal uptake in the rhizosphere, while preserving plant integrity and
primary functions, is a form of species tolerance to metals (Arduini et al. 1996; Verkleij
and Schat 1990). Plants can immobilize metals by absorption and accumulation through
roots, adsorption on roots, or precipitation within the rhizosphere. This process reduces
metal mobility leaching into groundwater and also reduces metal bioavailability in taking
part of the food chain (Yoon et al. 2006; Conesa and Faz 2011).
The four species present low TF values (<1) for As, obeying to the following order of
translocation ability (Fig. 6): Cytisus multiflorus, followed by Agrostis delicatula and Ulex
europaeus; Erica arborea has the lowest TF (0.190). As previously established, this may
be a favorable feature when considering the use of these plants in revegetation programs in
contaminated areas with As (Wong 2003). They all behave similar regarding Zn, with TF
around 1.1. In general, lower TF were observed for As and Cu, which suggests the plants’
 1100 P. GOMES ET AL.
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Figure 6 Translocation factor (TF) of the different species sampled for each element. Black bars on columns are
standard error (n = 3–7).

ability to retain them in the root system. On the other hand, higher TF were determined for
Mn, around 4.0, with the exception of Erica arborea (TF = 0,65).

CONCLUSION
The mineralogical characteristics of each site determine the metal and metalloid
concentrations in the waste dumps. The total metal concentrations in the three sites is
phytotoxic (>0.1%), which indicates that potential risk may still remain due to past mining
activities.
Mining waste texture and composition are known to influence the natural revegetation
success. However, in the three studied cases sand and silt sizes prevail with very small and
identical clay particle content.
The plant species analyzed showed high metal concentrations in their biomass.
Agrostis delicatula behaved as a bioaccumulator species, with BF>1 for all analyzed el-
ements. Erica arborea, Ulex europeaus, and Cytisus multiflorus had different behaviors
according to the concerned metal. They have BF < 1 only for As. Ulex europeaus accumu-
lates mainly Pb. Regarding TF, low values were obtained for most of the metals, especially
for As (TF < 1).
Combining data from metal concentration in biomass with BF and TF values, sug-
gest that the four species are prepared for the phytostabilization of the respective sites.
Therefore, using these plants could provide better conditions for natural attenuation or con-
taminant stabilization in the soil. This study indicates that enhancing conditions for natural
revegetation may be an appropriate and cost-effective strategy for remediation of these
sites, as well as for other small-medium size waste dumps located in similar conditions.
 METAL UPTAKE AND REVEGETATION OF WASTE-DUMPS 1101

ACKNOWLEDGMENTS
The authors acknowledge and appreciate the comments and suggestions made by the
Editor in Chief, Dr. Ebbs, and by four anonymous reviewers, which have helped to improve
the manuscript.

FUNDING
CIG-R is supported by the national budget of the Portuguese Republic through FCT –
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under the project PEst-OE/CTE/UI0697/2011.

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