Science of the Total Environment 542 (2016) 809–816

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Science of the Total Environment

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Screening of native plant species for phytoremediation potential at a

Hg-contaminated mining site
José Marrugo-Negrete a, Siday Marrugo-Madrid a, José Pinedo-Hernández a,
José Durango-Hernández a, Sergi Díez b,⁎
a
University of Córdoba, Faculty of Basic Sciences, Department of Chemistry, Water, Applied and Environmental Chemistry Group, Laboratory of Toxicology and Environmental Management,
Montería, Colombia
b
Environmental Chemistry Department, Institute of Environmental Assessment and Water Research, IDÆA-CSIC, E-08034 Barcelona, Spain

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Phytoremediation of Hg in native plants

was examined at a gold mining site.
• Atmosphere Hg concentrations must be
considered when assessing plant up-
take.
• Thus, the Translocation Factor does not
characterise plant uptake capacity.
• In gold mining sites, bioconcentration
and accumulation are the best factors
to use.
• Herbs and sub-shrubs are promising
native plants for remediation.

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

Article history: Artisanal and small-scale gold mining (ASGM) is the largest sector of demand for mercury (Hg), and therefore,
Received 1 June 2015 one of the major sources of Hg pollution in the environment. This study was conducted in the Alacrán gold-
Received in revised form 19 October 2015 mining site, one of the most important ASGM sites in Colombia, to identify native plant species growing in Hg-
Accepted 23 October 2015
contaminated soils used for agricultural purposes, and to assess their potential as phytoremediation systems.
Available online 7 November 2015
Twenty-four native plant species were identified and analysed for total Hg (THg) in different tissues (roots,
Editor: D. Barcelo stems, and leaves) and in underlying soils. Accumulation factors (AF) in the shoots, translocation (TF) from
roots to shoots, and bioconcentration (BCF) from soil-to-roots were determined. Different tissues from all
Keywords: plant species were classified in the order of decreasing accumulation of Hg as follows: roots N leaves N stems.
Translocation THg concentrations in soil ranged from 230 to 6320 ng g−1. TF values varied from 0.33 to 1.73, with high values
Accumulation in the lower Hg-contaminated soils. No correlation was found between soils with low concentrations of Hg and
Bioconcentration plant leaves, indicating that TF is not a very accurate indicator, since most of the Hg input to leaves at ASGM sites
Soils comes from the atmosphere. On the other hand, the BCF ranged from 0.28 to 0.99, with Jatropha curcas showing
Gold mining
the highest value. Despite their low biomass production, several herbs and sub-shrubs are suitable for
Jatropha curcas
phytoremediation application in the field, due to their fast growth and high AF values in large and easily harvest-
Colombia
able plant parts. Among these species, herbs such as Piper marginathum and Stecherus bifidus, and the sub-shrubs

⁎ Corresponding author.
E-mail address: sergi.diez@idaea.csic.es (S. Díez).

http://dx.doi.org/10.1016/j.scitotenv.2015.10.117
0048-9697/© 2015 Elsevier B.V. All rights reserved.
810 J. Marrugo-Negrete et al. / Science of the Total Environment 542 (2016) 809–816

J. curcas and Capsicum annuum are promising native plants with the potential to be used in the phytoremediation
of soils in tropical areas that are impacted by mining.
© 2015 Elsevier B.V. All rights reserved.

1. Introduction cover, which increases erosion. Furthermore, in many areas exploited

Mercury (Hg) is a naturally occurring element that is found in air,
water, and soil, and is a toxic environmental pollutant, since it can
cause severe damage to humans and wildlife (Díez, 2009). The primary
means by which humans are exposed to Hg are through the consump-
tion of contaminated food (methylmercury, MeHg, especially fish) and
the inhalation of air (mainly elemental Hg, Hg0). These two chemical
forms of Hg are of particular interest regarding artisanal small-scale
gold-mining (ASGM) areas (Steckling et al., 2011). Mercury is used to
extract gold from ore and is discharged in a vaporised form (Hg0) into
the environment, where it poses a hazard to human health. Moreover,
once released to environment, Hg undergoes a series of complex trans-
formations and cycles (e.g., biotic and abiotic methylation of inorganic
mercury) that produce MeHg, which fish accumulate from water
(Carrasco et al., 2011).
In Colombia, the largest gold-mining area is located in northern
Antioquia and southern Bolívar, and emissions to the atmosphere are
~ 80 to 100 t of Hg per year (Telmer and Veiga, 2008; Veiga, 2010;
Cordy et al., 2011). According to data from Cordy et al., 2011, approxi-
mately 130 t of metallic Hg was imported into Colombia in 2009. The
Alacrán gold mine is located in the Basin of the San Jorge River, Depart-
ment of Córdoba, where Hg is used in the amalgamation process for the
recovery of the precious metal (Marrugo et al., 2007) during the ASGM
process. Improper handling of Hg has led to the contamination of many
environmental compartments, threatening surrounding towns; a repre-
sentative case is the Santa Cruz mine in the Bolivar department, where
high Hg concentrations in humans have been reported (Olivero and
Johnson, 2002).
Artisanal and small-scale gold mining cause alterations of the local
ecosystems, and generates serious public health problems, because
once released, Hg can be transported from the soil and bodies of water
to humans (Islam et al., 2007). This type of mining is also considered
very detrimental to the environment, due to the removal of vegetation
by mining, this activity results in the emergence of a mosaic of second-
ary plant communities in different successional stages, according to the
time and intensity of disturbance (Díaz and Elcoro, 2009). Some authors
(cf. Ash et al., 1994) have indicated that the presence of plant commu-
nities at a particular site depends on the potential for seedlings to sur-
vive and reproduce. Establishment of plant species in contaminated
soils indicates that they are adapted to the contaminant and as such,
can remove or retain it, reducing its toxicity in soil (Chaney et al., 2000).
Plants known as hyperaccumulators can tolerate, absorb, accumu-
late, and translocate high levels of heavy metals (Chen et al., 2001;
Thangavel and Subhuram, 2004); and have been used in
phytoremediation, to remove, accumulate, and inactivate these con-
taminants (Padmavathiamma and Li, 2007).
Our research hypothesis was that through the identification of the
specific flora at the El Alacrán mine, we could identify the most useful
plant species for the phytoremediation of Hg in soils used for agricultur-
al purposes, and identify potential impacts based on the plant use
(Table 1). The aim of this study was to identify autochthonous plants
growing on a mining Hg-contaminated site, to assess their potential as
phytoremediation systems. To this end, we determined THg content in
different tissues (roots, stems and leaves), in the underlying soil sam-
ples, and Hg translocation (TF) and bioconcentration factors (BCF) in
the plants. A further aim was to analyse these factors in more detail
prior to making decisions concerning suitable plant selection for en-
hanced phytoremediation of Hg in mining areas.
2. Materials and methods
2.1. Study area
This study was conducted at the Alacrán mine (Fig. 1), located in the
upper part of the basin of San Jorge River at 7°44′29.01″N to 75°44′10.8″
W. First, the three-dimensional area occupied by the El Alacrán mine

Table 1
Collection of the autochthonous plant species reported in the Alacrán mine.

Family Scientific name Codea GH Utility

Bignoniaceae Tabebuia rosea L. 4950 Tree Wood

Cecropiaceae Cecropia peltata L. 4937 Tree Wood
Cyperaceae Cyperus ferax L. 4956 Herb Weeds
Cyperaceae Cyperus luzulae Retz. 4940 Herb Weeds
Cyperaceae Eleocharis interstincta (Vahl) Roem. 4941 Aquatic herb Ornamental, artisanal
Cyperaceae Oxycaryum cúbense Poepp & Kunth. 4957 Herb Weeds
Euphorbiaceae Jatropha curcas L. 4942 Sub-shrub Ornamental, fences of properties
Euphorbiaceae Phyllantus niruri L. 4943 Sub-shrub Medicinal
Euphorbiaceae Ricinus communis L. 4944 Sub-shrub Ornamental, medicinal
Fabaceae Inga spp. 4945 Tree Ornamental, artisanal, food
Fabaceae Senna alata L. 4946 Shrub Degraded soils recovery
Gleicheniaceae Stecherus bifidus Willd. 4947 Herb Ornamental
Lamiaceae Plectramthus spp. 4948 Herb Medicinal, ornamental
Malvaceae Ceiba pentandra L. 4952 Tree Wood
Malvaceae Guazuma ulmifolia L. 4955 Tree Artisanal, cattle food
Marantaceae Thalia geniculata L. 4938 Aquatic herb Ornamental, artisanal
Marantaceae Calathea lutea Aubl. 4958 Herb Cultural, artisanal housing construction
Melastomataceae Clidemia sp. 4949 Shrub Ornamental
Mutingiaceae Mutingia calabura L. 4951 Shrub Ornamental, sweet fruit
Myrtaceae Psidium guajaba L. 4939 Tree Ornamental, food
Onagraceae Ludwigia octovalvis L. 4960 Herb Weeds
Piperaceae Piper marginathum L. 4953 Herb Ornamental
Pteridaceae Pytirogramma colomelanos Kaulf. 4954 Herb Ornamental
Solanaceae Capsicum annum L. 4959 Sub-shrub Food

GH: growth habit.

a
Code of the plants deposited in the Herbarium of the University of Córdoba (HUC).
 J. Marrugo-Negrete et al. / Science of the Total Environment 542 (2016) 809–816
Fig. 1. Maps of Colombia and the San Pedro river basin, with the location of the Alacran gold mining site, Department of Córdoba.
was determined. This included mapping the slope and drainage, and
runoff directions using ArcGIS software version 9.3.1.
The total area of exploitation (or the area of intervention) of the
mine that has been in operation since the 1970s, is 23.5 km2 (Fig. 1).
Local miners transport and accumulate tonnes of gold ore that are
mined in the surrounding hills, to Alacrán Village. Gold ore is processed
in processing centres or entables that are located beside residences,
schools, and stores. These entables operate in the village and amalgam-
ate the whole ore and burn gold amalgam without any filtering or con-
densing system. Miners and residents of the town are classified as rural,
with a low education level, poor socio-economic status, and a low cov-
erage of programmes developed by the national government (Doria
et al., 2013).
2.2. Sample collection
During sample collection along a linear transect (Fig. 1) samples of
soil and the most common plant species were selected at each site. At
each site, three adjacent plots were randomly chosen and at each plot,
one plant was randomly selected. Under the canopy of the same plant,
topsoil samples were collected (one composite sample obtained from
three sub-samples). In total, 72 samples of roots, stems and leaves and
72 samples of soil were analysed: one plant and soil sample per plot,
for three plots, at 24 sites. All soil samples were collected from the top
layer (0–20 cm) using a stainless steel spade whilst wearing clean sam-
pling gloves; three soil subsamples were collected from the same area
where the plant sample was collected, and were mixed and
homogenised to create a composite sample. The composite sample
was placed in a labelled clean polyethylene plastic bag, and was
transported to the laboratory in a covered cooler with ice packs. In the
laboratory, soil samples were air-dried at room temperature to constant
weight, and were mixed well to homogenise the soil. Finally, samples
811
were crushed and sieved to b 2 mm to remove stones and roots, and
were stored in labelled sealed plastic bags in a refrigerator.
Three plants of each plant species were collected using clean dispos-
able gloves and were placed into individual paper bags. Samples were
kept cool and moist after collection, and were placed in a cooler with
ice packs to store them during on-site sampling, and were transported
to the laboratory as soon as possible. Once in the laboratory, fresh plants
were pressed in newsprint, for taxonomic determination in the herbar-
ium of the University of Córdoba (HUC), using specialised literature
(Geantry, 1995). Plants were sorted by species and were thoroughly
washed with running tap water, and rinsed with deionised water to re-
move any sediment particles attached to the plant surface. The identity
of each specimen was determined in the HUC and was referenced with
the codes 4937–4960. Twenty four species of plants were reported,
which were grouped into 16 families. Plant tissues were separated
into roots, stems, and leaves, and were dried at 40 °C in a forced convec-
tion oven. They were then placed in labelled sealable plastic bags and
stored in a cool (4 °C), dark and dry environment until analyses.
Different surveys were carried out in the Alacrán mine area (i.e., area
of intervention and the Alacrán village) with the aim of describing the
Hg content in the air–soil system. Atmospheric Hg emissions were stud-
ied using gaseous mercury (TGM) surveys, including 995 TGM determi-
nations. Data were obtained by Zeeman effect Atomic Absorption
Spectrometry with the High Frequency Modulation technique (ZAAS-
HFM), using a number of LUMEX-RA-915 series devices (Sholupov
et al. 2004).
2.3. Sample analysis
For the analyses of THg in plants, approximately 0.5 g plant material
(dry weight basis, dw) was subjected to assisted digestion by a micro-
wave with a mixture of HNO3/H2O2 (5:2) (Jedrzejczak et al., 1996). Sim-
ilarly, 0.5 g soil dw was microwave-digested using 10 mL 65% HNO3
812 J. Marrugo-Negrete et al. / Science of the Total Environment 542 (2016) 809–816

solution according to the EPA method 3051A (USEPA, 2007). The micro-
wave oven used was a Milestone ETHOS TOUCH 127697 series with a
temperature range of 100–175 °C and a pressure of 1500 kPa. The THg
was determined by cold vapour atomic absorption spectroscopy (CV-
AAS) using a Thermo Scientific iCE 3000 series analyser. Analytical qual-
ity control of the methods was evaluated in triplicate with certified ma-
terials for tomato leaves (CRM 1753a, 34 ng g− 1), and soil/sediment
(CRM008–050, 720 ng Hg g−1), and the percentage recovery was 98%
and 97%, respectively. The detection limit for THg was 14 ng g−1 dw,
calculated as three times the standard deviation (SD) of the blank.
The content of organic matter was determined as a percentage of the
loss by ignition of 2.0 g soil in a furnace at 450 °C (Muffle furnace
Terrígeno D8) for 4 h (Coquery and Welbourn, 1995). The pH of the
soil was measured using a WTW, 330i pH meter.
2.4. Translocation, bioconcentration, and accumulation factors
BCF and TF factors were estimated using the determined Hg concen-
trations. The BCF was expressed as the ratio of the metal concentration
in the roots to that in soil (Yoon et al., 2006). The TF for the metals with-
in a given plant was calculated as the ratio of the metal concentration in
the shoots to that in the roots (Zu et al., 2005). Plants with a BCF and TF
both greater than one (TF and BCF N 1) have the potential to be used for
phytoextraction (Raskin and Ensley, 2000; Yoon et al., 2006). Moreover,
to optimise and improve the phytoremediation process, the optimum
scenario is to concentrate the metal(s) in the above-ground portion of
the biomass, and to harvest and recover metals from the biomass, if
practical (Jee, 2007). For this, the accumulation factor (AF), calculated
as a ratio of metal in the harvestable part of the plant (i.e., shoots) to
that in the soil, is required for the design considerations of
phytoremediation systems.
2.5. Statistical analysis
Analyses of THg in tissues and soils was reported as the mean ± SD
of triplicate determinations from three plants and three soils (Table 2).
Initially, data were log-transformed, and normality tests (Ryan–Joiner)
and variance homogeneity (Levene) were applied. The Spearman corre-
lation was performed to establish relationships between variables using
the statistical software Statgraphics Centurion 15.2.06. The criterion for
significance was set at p b 0.05.
3. Results and discussion
3.1. Floristic composition
The floristic composition of the Alacrán mine, based on its character-
istics and usefulness, is shown in Table 1. Twenty-four species were ob-
served and grouped into 16 families. Most of the inventoried species in
the El Alacrán mine are common for areas disturbed by mining (Díaz
and Elcoro, 2009) and in general, these species are characterised by
rapid growth, and those in the Cyperaceae family are considered to be
pioneer species during colonisation at the creation of an ecosystem
(Reyes et al., 2006).
These herb species, shrubs and sub-shrubs that are representative of
the Euphorbiaceae family (Jatropha curcas, Phyllanthus niruri, Ricinus
communis), Solanaceae (Capsicum annuum) and Piperaceae (Piper
Marginathum) are common in mining areas of tropical regions, and be-
come established after several months of mining activity (Reyes et al.,
2006). In isolation, we also observed tree species that exist in a primary
forest, particular in rainforests, consisting of Tabebuia rosea, Ceiba
pentandra and Cecropia peltata.
3.2. THg in soils
Mercury is naturally present in soils at concentrations ranging from
0.003 to 5 mg/kg (Steinnes, 1997), although in most cases, is below
0.5 mg/kg (Schlüter, 1993). The THg in soils of the El Alacrán mine are
shown in Table 2. The concentrations are relatively low (range
230–6320 ng g−1) compared to other Hg-contaminated areas world-
wide, such as the mining district of Almaden in Spain
(0.13–2695 μg g− 1) (Molina et al., 2006), or Santa Cruz mine in
Colombia (500–30,000 ng g− 1) (Pérez-Castro, 2010), but are higher
than values for Colombian soils and soils engaged in agriculture
(Alloway, 2005). Moreover, according to UNEP (UNEP, 2002), prelimi-
nary critical limits to prevent ecological effects due to Hg in organic
soils have been set at a soil THg content of 0.07–0.30 mg/kg. Taking
into account that elevated Hg concentrations were found in some

Table 2
Mean and standard deviation (±SD) of total mercury (THg) in soils (n = 3) and tissues of the plant species (n = 3) reported in the Alacrán mine, Colombia. Translocation (TF),
bioconcentration (BCF) and accumulation (AF) factors are also reported.

Family Scientific name THg (ng g−1) TF BCF AF

Soil Root Stem Leaf

Euphorbiaceae Jatropha curcas 6022 ± 3 5983 ± 2 954.1 ± 0.6 2782 ± 1 0.62 0.99 0.62
Marantaceae Thalia geniculata 4077 ± 4 3696 ± 2 429.0 ± 0.7 979.2 ± 0.2 0.38 0.91 0.35
Piperaceae Piper marginathum 5130 ± 3 4685 ± 4 525.6 ± 0.5 2178 ± 1 0.58 0.91 0.53
Cyperaceae Cyperus ferax 3676 ± 4 3216 ± 4 235.6 ± 0.2 852.1 ± 0.4 0.34 0.87 0.30
Euphorbiaceae Ricinus communis 6267 ± 5 5205 ± 2 649.8 ± 0.1 1900 ± 1 0.49 0.83 0.41
Pteridaceae Pityrogramma colomelanos 401.5 ± 2.2 333.4 ± 0.4 75.2 ± 0.8 108.2 ± 0.6 0.55 0.83 0.46
Solanaceae Capsicum annuum 340.4 ± 1.7 284.1 ± 0.6 109.5 ± 0.5 229.2 ± 0.3 1.19 0.83 1.00
Gleicheniaceae Stecherus bifidus 1268 ± 4 1018 ± 4 231.3 ± 0.4 535.6 ± 0.7 0.75 0.80 0.61
Malvaceae Guazuma ulmifolia 228.5 ± 0.5 174.3 ± 0.3 46.4 ± 0.4 68.6 ± 0.2 0.66 0.76 0.50
Fabaceae Senna alata 226.5 ± 2.1 169.8 ± 0.1 63.6 ± 0.2 71.7 ± 0.5 0.8 0.75 0.60
Bignoniaceae Tabebuia rosea 4970 ± 3 3633 ± 4 547.4 ± 0.5 1018 ± 1 0.43 0.73 0.31
Marantaceae Calathea lutea 1692 ± 4 1226 ± 6 185.1 ± 0.7 499.6 ± 0.8 0.56 0.72 0.40
Cyperaceae Eleocharis interstincta 490.1 ± 2.9 341.1 ± 0.2 84.3 ± 0.8 177.2 ± 0.9 0.77 0.70 0.53
Cecropiaceae Cecropia peltata 1503 ± 4 1033 ± 2 147.8 ± 0.2 204.7 ± 0.4 0.34 0.69 0.23
Cyperaceae Oxycaryum cúbense 729.8 ± 2.1 496.4 ± 0.7 123.4 ± 0.4 222.2 ± 0.3 0.7 0.68 0.47
Euphorbiaceae Phyllanthus niruri 319.6 ± 2.1 187.2 ± 0.3 62.2 ± 0.4 147.5 ± 0.7 1.12 0.59 0.66
Myrtaceae Psidium guajava 6322 ± 4 3419 ± 7 722.5 ± 0.9 958.4 ± 0.5 0.49 0.54 0.49
Cyperaceae Cyperus luzulae 340.5 ± 1.8 159.5 ± 0.4 63.7 ± 0.4 88.5 ± 0.2 0.95 0.47 0.45
Malvaceae Ceiba pentandra 3214 ± 2 1257 ± 3 153.4 ± 0.6 260.5 ± 0.2 0.33 0.39 0.13
Muntingiaceae Muntingia calabura 395.7 ± 1.4 154.1 ± 1.4 28.7 ± 0.2 86.1 ± 0.8 0.74 0.39 0.29
Melastomataceae Clidemia sp. 650.8 ± 5.4 234.1 ± 1.2 111.3 ± 0.4 221.1 ± 0.7 1.43 0.36 0.51
Lamiaceae Plectramthus sp. 444.3 ± 5.9 145.9 ± 2.4 104.5 ± 0.6 148.5 ± 0.6 1.73 0.33 0.57
Onagraceae Ludwigia octovalvis 494.6 ± 1.1 149.4 ± 0.2 53.2 ± 0.4 87.9 ± 0.5 0.94 0.30 0.29
Fabaceae Inga edulis 631.1 ± 3.3 179.4 ± 0.4 84.7 ± 0.6 132.3 ± 0.7 1.21 0.28 0.34
 J. Marrugo-Negrete et al. / Science of the Total Environment 542 (2016) 809–816
soils, in some cases ~20 times higher than the UNEP recommendation,
their use for livestock farming and agricultural crop production poses
a threat to public health, and indicates that there is a need for
remediation.
The soils were acidic (range 4.15–4.09) with low organic matter con-
tents (3.04 to 3.56%). Based on these soil properties, Hg should be more
mobile and more bioavailable, because organic-rich soils lead to a lower
bioavailability and mobility of metals than those present in mineral soils
(Olaniran et al., 2013), whereas at low pH values, metals are present as
free ionic species or as soluble organo-metals, and these are more bio-
available (Sandrin and Hoffman, 2007).
Soils were characterised as having low (230–500 ng g−1), medium
(630–1700 ng g− 1) or high (3200–6320 ng g− 1) Hg concentrations
(Fig. 1). The highest Hg concentrations in soils were found near the
entables of Alacrán village (~ 0.5 km), with concentrations about 25
times higher than in the area of extraction (~ 1.0 to 1.5 km distant).
Moreover, the runoff streams might carry loads with a high Hg concen-
tration. In fact, effluents from the El Alacrán mining area poured into the
basin of San Pedro River, where the content of Hg in sediment samples
(916 ± 7 ng g−1) and surrounding soils (780 ± 2 ng g−1) increases con-
tinuously, especially due to flooding.
3.3. Mercury accumulation in plants
Concentrations of THg in different plants tissues are shown in
Table 2. These species are distributed in the soils of El Alacrán mine
and accumulate Hg concentrations in their tissues, indicating that
these plants are adapted to contaminated soils.
For all species, the root accumulated the most Hg, followed by the
leaves and the stem, which agrees with other studies (Molina et al.,
2006; Marrugo-Negrete et al., 2015). The amount in the roots was 2.5-
and 5-fold higher than in the leaves and the stems, respectively, where-
as the leaf concentration was twice as high as in stems. A low distribu-
tion of Hg to the shoots was also found in other plant species (Wang
and Greger, 2004), which is probably due to the high affinity of roots
for Hg, by trapping most of the bioavailable Hg. This is because the
roots are directly exposed to Hg in the soil, which mostly is accumulated
in the cell walls, to avoid toxic effects on the aerial parts, especially the
development of necrosis and chlorosis in leaves (Marrugo-Negrete
et al., 2015).
Notably, Hg concentration was higher in the leaves than in the
stems. The main function of the stems is to transport fluids and nutri-
ents between the roots and the leaves in the xylem and phloem. One ex-
planation for the lower Hg concentrations in the stems might be the
result of this transport function, which does not allow Hg to accumulate,
and instead, facilitates its transport to the aerial parts of the plant for
more permanent storage.
Additionally plant leaves can accumulate Hg from the air. Reported
small-scale experiments indicate that plants can act as both a source
and sink of atmospheric Hg (Leonard et al., 1998; Schwesig and
Matzner, 2000), and can also transport 10% of the total soil Hg to the fo-
liage (Bishop et al., 1998). More recently, Gustin et al., 2004, demon-
strated that for vegetation growing in soil with an elevated Hg
concentration and exposed to elevated air concentrations, the vegeta-
tion acts as a sink for atmospheric Hg, and shading of the soil reduces
emissions from soils. Almost all of the Hg in foliar tissue originates
from the atmosphere (Ericksen et al., 2003), and the root concentrations
reflect the soil Hg concentration (Frescholtz et al., 2003; Cocking et al.,
1995). It is thought that little Hg passes from the roots to the above-
ground component of the plant. Godbold (1988) proposed that al-
though high Hg concentrations might exist in the roots, very little
translocation to the stem occurs, because Hg binds tightly to the cell
walls in the root.
In summary, plants transmit Hg from the soil to the air via the tran-
spiration stream (Leonard et al., 1998), but according to Frescholtz et al.
(2003), leaves accumulate atmospheric Hg as a function of the air
813
concentration. They also found that soil Hg concentration influenced
the leaf Hg concentration, and indicated that the soil Hg concentration
had a greater influence on foliar Hg concentration when the air Hg con-
centration is low, which is not the case in the Alacrán gold-mining area,
where air Hg concentrations have been found to range from 1 to
46,000 ng m−3.
The practise of separating Hg from gold by burning the amalgam in a
pan with a blowtorch results in very high direct losses of Hg to the at-
mosphere. Local miners carry gold ore from the mine to the entables
in the urban environment. Commonly, miners in entables do not pre-
concentrate the ore, and Hg is added to the whole high-grade material
in small ball mills, known as cocos. This whole ore amalgamation pro-
cess maximises Hg losses in tailings and effluent (Cordy et al., 2011;
Schmidt, 2012). As described by these studies, the air Hg concentration
in these entables is occasionally nearly 1000 times the World Health
Organisation's (WHO) air quality guideline of 1 μg m−3 for chronic ex-
posure to inorganic Hg vapour (WHO, 2012) and 3000 times the U.S. En-
vironmental Protection Agency reference concentration of 0.3 μg m−3
for chronic inhalational exposure to inorganic Hg (USEPA, 1995). Total
gaseous mercury concentrations (TGM) in the gold-mining area ranged
from 1 to 46,000 ng m−3. The highest values were found in the village,
inside gold shops (530–46,000 ng m−3) and in the entables
(1900–4000 ng m− 3) (Higueras and Marrugo, unpublished results).
Values of TGM close to the mine are similar to background values
(1–110 ng m−3), which are much higher than usual background values
(~2 ng m−3) (Higueras et al., 2014). Therefore, the TGM concentrations
were above the WHO maximum recommended level and the U.S. EPA
reference concentration for chronic exposure. It should be thus
highlighted that in some areas of the Alacrán gold mine site, airborne
Hg concentrations are more significant than soil Hg concentrations.
The relationship between the amount of Hg accumulated by plants
and the content in the soil can depend on the taxon (Boening, 2000).
A significant correlation was observed between the Hg concentration
in the soil and that in different plant tissues (Fig. 2). THg content in
the soil was statistically significantly correlated with the Hg content
analysed in the 24 species, in the roots (r = 0.96, p b 0.05), stems
(r = 0.94, p b 0.05), leaves (r = 0.87, p b 0.05), and shoots (r = 0.90,
p b 0.05). Thus, the accumulated Hg in the tissues of plants in the
Alacrán mine is directly related to the content of Hg present in the soil
and air due to gold-mining activities. Notably, higher correlations
were found for roots, followed by stems and then leaves, which differs
from the pattern for the relative Hg absorption by plant tissues, which
was in the decreasing order: roots N leaves N stems.
As previously mentioned, emissions of Hg in the air at the ASGM site
are high, and are comparable to those at other ASGM sites in Colombia,
Fig. 2. Correlation between Hg content in soils with roots, leaves, stems and shoots of au-
tochthonous plants (n = 24) at the Alacrán gold mine.
814 J. Marrugo-Negrete et al. / Science of the Total Environment 542 (2016) 809–816
such as the Santa Cruz or San Martin de Loba mines, where airborne
values range from 164 to 40,500 ng m−3 and 220 to 27,000 ng m−3, re-
spectively (Olivero et al., 2014). Therefore, the increase in the Hg bur-
den in plant leaves due to atmospheric deposition might explain the
lower correlation found between soil and leaves, in comparison with
that in soil versus roots and/or stems, because the air concentration
fluctuates over time.
We hypothesise that one of the contributing causes to the lower cor-
relation between soils and shoots is the increase in the Hg burden in the
leaves that receive external inputs (i.e., atmospheric assimilation
through the stomata and leaf cuticle) (Molina et al., 2006). This hypoth-
esis has been corroborated by the fact that at elevated Hg concentra-
tions in soil (1270 to 6320 ng g−1), the correlation with leaves is high
and significant (n = 11; r = 0.75; p b 0.05), whereas in the lower con-
centration range (230 to 650 ng g−1), the correlation is moderate (n =
11; r = 0.4; p = 0.23) and not significant. This indicates that Hg in the
leaves in plants growing in soil with a low-concentration of Hg derives
primarily from the air, since no significant correlation with soil exists.
3.4. Translocation and bioconcentration factors
To evaluate the ability of all plant species to translocate Hg from the
roots to the aerial parts of the plant, the TF was calculated (Table 2). As
several authors have reported (Tu et al., 2003), translocation of Hg from
the roots to the aerial parts of the plant (i.e., the shoots) occurs when the
TF is higher than 1. Only five plants, from four different families had a TF
value greater than one. The highest value (1.73) was shown by a plant
from the Lamiaceae family (Plectramthus sp.). The TF value (1.43) for
Clidemia sp. also indicated that Hg is highly transferable for this plant
(Fig. 3). However the experimental design used in this study did not
allow the Hg in plant leaves from the two sources to be distinguished,
i.e., uptake from the air or transport from the roots. These results sug-
gest that in soils with lower Hg concentration, where the atmospheric
inputs are probably more significant than Hg translocation from the
roots, the information derived from the TF is not particularly useful.
On the other hand, BCF measures the relationship between the metal
Fig. 3. Translocation (TF) and bioconcentration factors (BCF) for native plants species growing in the Alacran gold mine site.
concentration in the plant and the metal concentration in the under-
lying soil. In all cases, BCFs value was less than one, indicating that
Hg was transferred to the plant, but not to a significant extent
(Ruíz and Armienta, 2012). The highest value (0.99) was observed
for J. curcas, and Thalia geniculata and P. marginathum have suffi-
ciently high values (0.91) to be considered good accumulators. Fur-
thermore, other good candidates such as C. annuum, Pityrogramma
colomelanos and R. communis, should not be disregarded (marked
by a dashed line in Fig. 3). In summary, among the recorded species,
J. curcas, P. marginathum, T. geniculata, Cyperus ferax or C. annuun
displayed a significant increase in the efficiency of Hg bioaccumula-
tion, with J. curcas representing the best potential candidate for
phytoremediation. Studies with J. curcas seedlings (Gao et al.,
2010) demonstrated that Hg accumulates during germination, with
a higher content in the radicle than in the cotyledons and hypocotyl
and this species also accumulates other heavy metals, showing the
best absorption capacity for Cd, Cr, Ni, and Zn in the roots (Chang
et al., 2014). However, other species have been assessed for their
phytoremediation potential, such as R. communis, which has been
used to remediate lead (Pb) with more storage capacity in the aerial
parts (Rodríguez et al., 2006), or C. peltata (Vidal et al., 2010), which
accumulates large amounts of Hg without showing toxic effects.
3.5. Plant selection for phytoremediation in the field
Phytoremediation offers significant cost advantages over alternative
technologies of soil excavation and treatment or disposal. In addition,
the use of native plants reduces the costs of mowing, replanting, prun-
ing and harvesting, with the added benefit of not disturbing the soil if
the accumulation of potentially toxic metal(s) occurs in easily harvest-
able plant parts (mainly shoots).
Many factors contribute to the suitability of identified plants
for phytoremediation of Hg in the Alacrán mine area. According
to McGrath and Zhao (McGrath and Zhao, 2003), phytoextraction effi-
ciency is determined by two key factors: the ability to accumulate
metals and biomass production. Consequently, design considerations
 J. Marrugo-Negrete et al. / Science of the Total Environment 542 (2016) 809–816
of phytoremediation systems include the accumulation factor (AF) (the
ratio of metal in the shoots to that in the soil) and plant productivity
(biomass that is harvestable). In terms of cost-effectiveness, it is prefer-
able that the metal accumulates in the shoots as opposed to in the roots,
because it can then be cut from the plant and removed; if the metal is
concentrated in the roots, the entire plant needs to be removed. Remov-
ing the metals simply occurs by pruning or cutting the aboveground
mass of the plant. Due to specific characteristics at ASGM sites, where
the shoots accumulate Hg from both the soil and from the air, a fast-
growing plant that is easily harvested and that accumulates large con-
centrations of Hg in harvestable tissues is ideal.
Firstly, a knowledge on the abundance of the plant species,
together with the AF is necessary to select the most suitable plants
for phytoremediation. The operation and maintenance costs of
phytoremediation could be reduced, depending on the selection of
native plants.
In this study, eleven of the reported species are herbaceous
(Table 1), which indicates that the areas studied were colonised rapidly
and from the ecological point of view, these wild plants should be con-
sidered abundant in this ecosystem. This group contains two aquatic
plants (e.g., Eleocharis interstincta and T. geniculata), and the latter
grows in flooded soils (with high levels of Hg) due to contaminated run-
off from the entables. Shrubs and sub-shrubs are representative of the
Euphorbiaceae, Solanaceae and Piperaceae families (seven species in
total), with J. curcas, R. communis and P. marginathum, growing in the
most polluted soils. Finally, trees are unrepresentative species, with a
more limited abundance and consist of perennial species, such as
T. rosea, C. pentandra and C. peltata species, which grow in high-Hg
soils, particularly in the rainforest.
Different plant species displayed similar trends of accumulation (i.e.
AF values) to those of BCF, with maximum values shown by herb and
sub-shrub species. The highest accumulation was found for the sub-
shrub C. annum and the other values ranged from 0.66 to 0.13. Some
trees, such as Guazuma ulmifolia and Psidium guajaba showed relatively
high AF values (~0.50).
In summary, herbaceous and sub-shrubs species are the most repre-
sentative plant groups, which are characterised by fast-growing (Reyes
et al., 2006), large round leaves, and a high accumulation of Hg, and
therefore, they appear to be suitable for remediation purposes through
removal of the aerial parts of the plant. Although herbs and sub-shrubs
are the most abundant and effective phytoextractors, they usually pro-
duce less biomass. Although they accumulate less Hg, trees can be
very effective phytoremediators, due to their higher biomass, since
plants with a high biomass production capacity can compensate for
their relatively low metal accumulation capacity, and the extent of
metal removal can be even higher (Zhuang et al., 2007). In any case,
the use of trees should not be disregarded for phytoremediation in the
Alacrán mining site.
This study confirms that in addition to their ability to adapt to erod-
ed and mining soils, herbs (e.g., Stecherus bifidus and P. marginatum) or
sub-shrubs (e.g., C. annum and J. curcas) grow rapidly and have a rela-
tively high Hg accumulation in roots (BCF) and shoots (AF). In fact, pre-
vious studies in laboratory experiments with J. curcas showed that the
highest cumulative absorption of Hg occurs between the second and
third month of exposure (Marrugo-Negrete et al., 2015).
Finally, when dealing with remediation projects in zones affected
by mining activities, the risk posed by the ingestion of the plants by
fauna is often forgotten. Contamination can spread throughout the
food chain if plant tissues are ingested by animals. Moreover, some
plants that accumulate Hg have many uses among the inhabitants
of the San Jorge river basin (Table 1), and some are used even as food.
Considering the amount of Hg accumulated in some wild plants, their
use as food is not recommended. If possible, access to the site must be
controlled, as the plants may be harmful to livestock, wildlife, and
humans, and caution should be advised, especially if they are typically
consumed.
815
4. Conclusions
This study demonstrated alternatives for Hg soil decontamination
through the ability of autochthonous plant species to accumulate this
metal. Independently of the Hg concentration in the soil, different
plant species accumulated Hg in their tissues in the order: roots N
leaves N stems. The Hg content in their tissues indicates the storage ca-
pacity of these plants to accumulate Hg by transfer from the soil (BCF)
or within different parts of the plant (e.g., from roots to shoots), using
the TF. Nevertheless, due to the characteristics of ASGM sites, where
gold is separated from Hg by burning the amalgam, the atmospheric in-
puts to the plants leaves are expected to be more significant than Hg
translocation from the roots, and therefore, the information derived
from TF is not very useful. Although Hg in the atmosphere primarily in-
fluenced foliar uptake, root concentrations were related to the soil Hg
concentration. According to BCF and AF values, several plants were
identified as promising native plants to remediate Hg-contaminated
soils. Plant species established at the El Alacrán mine have different con-
centrations of Hg in their tissues, demonstrating that the accumulation
of contaminants depends on the morpho-physiological characteristics
of each species. The greatest accumulation of Hg was shown by shoots
of the species J. curcas, P. marginathum, C. annuum, and S. bifidus.
Among these, J. curcas showed the highest degree of Hg accumulation
in roots, and a high value in shoots, indicating its potential to be used
as a natural treatment to decontaminate soils in tropical areas impacted
by ASGM sites.
Acknowledgements
To the University of Córdoba, the Laboratory of Toxicology and Envi-
ronmental Management; COLCIENCIAS, for financing the project: “Re-
moval of mercury in soils by plants that grow in lands contaminated
with metal (El Alacrán mine in the Department of Córdoba and Santa
Cruz mine in the Department of Bolívar)”, identified with the code
111248925604 and contract number 472-2009. We appreciate the
anonymous reviewers and the Associate Editor for their valuable com-
ments and suggestions to improve the quality of the manuscript.
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