Communications in Soil Science and Plant Analysis, 42:2767–2777, 2011

Copyright © Taylor & Francis Group, LLC

ISSN: 0010-3624 print / 1532-2416 online
DOI: 10.1080/00103624.2011.622823

Mercury Mobilization in a Contaminated Industrial

Soil for Phytoremediation

FRANCESCA PEDRON,1 GIANNIANTONIO PETRUZZELLI,1

MERI BARBAFIERI,1 ELIANA TASSI,1 PAOLO AMBROSINI,2
AND LEONARDO PATATA2
1
National Research Council, Institute of Ecosystem Study, Pisa, Italy
2
Saipem/Risamb, Fano, Italy

The aim of this work was to investigate the possibility of using plants for mercury (Hg)
removal from a contaminated industrial soil, increasing the metal’s bioaccessibility by
using mobilizing agents: ammonium thiosulphate [(NH4 )2 S2 O3 ] and potassium iodide
(KI). The selected plant species were Brassica juncea and Poa annua. The addition of the
mobilizing agents promoted Hg uptake by plants, with respect to controls. Treatments
promoted Hg translocation to aerial parts. In the case of Poa annua, greater Hg uptake
was found in plants after the 100 mM KI treatment, reaching values that were nearly
400 mg kg−1 in the aerial part. In contrast, Brassica juncea plants accumulated in their
aerial part the greatest Hg quantities, about 100 mg kg−1 , after treatment with 0.27 M
(NH4 )2 S2 O3 . The ratio between the concentration of Hg in the shoots and the initial con-
centration in the soil support the potential for successfully applying Hg phytoextraction
on this soil.

Keywords Brassica juncea, Hg-mobilizing additives, Poa annua, pot experiments

Introduction
Mercury (Hg) is a highly toxic non-essential element and is considered a global envi-
ronmental pollutant because of its ability to undergo long-distance transportation in the
atmosphere (Wang, Shi, and Wie 2003; Boening 2000). The presence of Hg in the total
environment—soil, water, air, and biota—is due to natural and anthropogenic sources.
Inorganic Hg occurs naturally in very small amounts in oceans, rocks, and soils. It becomes
airborne from rock erosion, volcanic activity, and soil decomposition. There are also many
anthropogenic sources, from household and commercial products to industrial processes
(Pacyna and Pacyna 2002; Veiga and Hinton 2002). This metal can be released from coal-
fired power plants, municipal incinerators, some manufacturing plants, hospitals, dental
offices, schools, and even homes (fluorescent lights, thermostats, thermometers) (Hylander
and Herbert 2008). It can return to terrestrial ecosystems, in which the soil is the largest
Hg recipient, through both wet and dry deposition, in Hg(II) and Hg(0) forms, respectively,
and as much Hg particulate deposition (Morel, Kraepiel, and Amyot 1998).

Received 3 August 2010; accepted 15 May 2011.

Address correspondence to Francesca Pedron, National Research Council, Institute of
Ecosystem Study, Via Moruzzi 1, 56124, Pisa, Italy. E-mail: francesca.pedron@ise.cnr.it

2767
2768 F. Pedron et al.

In the soil, Hg chemistry is characterized by various reactions that involve adsorption

and release from solid phases, complexation with organic and inorganic ligands, oxida-
tion reduction, and methylation (Shuster 1991). Depending on the redox conditions, Hg
may exist in three valence states; Hg0 , Hg2+ , Hg2+ 2 . Mercury may be present in many
complexed forms with chloride (Cl− ), oxydril (OH− ), and sulfur (S) containing functional
groups of organic ligands according to pH, ionic strength, redox potential, and dissolved
organic matter in soil (Steinnes 1997). Many compounds of Hg with sulfide, mainly present
in anoxic environments, are highly stable and insoluble, while inorganic ligands such as
Cl− ions that form highly stable linkages with Hg promote the release of the element in the
soil liquid phase.
Mercury can also be present within terrestrial environments in the two common
methylated forms, methyl- and dimethyl-Hg (Compeau and Bartha 1985; Choi and Bartha
1993; Zhang and Planas 1994; Jackson 1998; Gavis and Ferguson 1972; Gabriel and
Williamson 2004). Although concentrations of these compounds in soil are low (in partic-
ular, methyl-Hg is less than 2% of the total Hg present in soil), they cause bioaccumulation
problems.
Soil properties that determine Hg retention by mineral and organic surfaces are mainly
pH and dissolved ions (Gabriel and Williamson 2004). Clayey and organic soils have the
greatest ability to adsorb Hg, which is also strongly retained by oxides, hydroxides, and
oxyhydroxides of iron (Fe), manganese (Mn), and aluminum (Al). If soils are neutral to
alkaline, Hg shows stronger adsorption to mineral components, while a decrease in pH
can, together or separately with an increase in chloride concentration, reduce the adsorption
processes of the metal (Shuster 1991). A decrease in Hg adsorption will also increase its
volatilization, which is strongly dependent on soil moisture, permeability, and temperature.
Sunlight intensity and ambient air temperature are positively correlated with the abiotic
reduction and volatilization of Hg from soil (Gustin, Biester, and Kim 2002).
The behavior of Hg in the soil environment is of great importance at contami-
nated sites, because the applicability of remediation technologies largely depends on the
chemical forms of Hg in soil. Because of Hg use in many industrial processes, several
contaminated sites exist in the world, and new techniques for remediation are under exam-
ination. Several technologies are available to remediate the pollution of Hg in the soil;
among these excavations, soil washing, and electroremediation are the most frequently
used in Europe, while phytoremediation appears to be an interesting low-cost alternative,
especially regarding the common practice of disposing soil contaminated by heavy metals
in landfills (Tandy et al. 2009).
Phytoextraction, the use of plants to remove non-degradable contaminants from
the soil, is considered an environmentally friendly technology that can be applied for
some heavy metals (Anderson, Moreno, and Meech 2005; McGrath et al. 2006; Arshad
et al. 2008; Tassi et al. 2008). Whether this strategy is suitable for the cleanup of Hg-
contaminated soil is still an open issue, because often the metal is not in a bioavailable
form in soil and plant tolerance to Hg is generally low.
The potential use of engineered plants (Meagher et al. 2000) to remediate Hg-
contaminated soils is not allowed by Italian legislation (2006); moreover, there is concern
about the release of Hg into the atmosphere when using phytoremediation with geneti-
cally modified plant species. An alternative to the use of transgenic plants is enhancing Hg
availability by the use of additives, taking care that the metal is not leached into deeper soil
horizons. This strategy has been explored in recent years by using new additives instead
of typical complexing agents such as ethylenediaminetetraacetic acid (EDTA), for which
there is a concern about negative environmental effects (Meers et al. 2005). With these
 Mercury Phytoextraction 2769

new additives, interesting results have been obtained by the use of thioligands (Moreno
et al. 2004, 2005a, 2005b) and halogen salts (Wang 2004), which are non-toxic chemicals
commonly used in agriculture for their fertilizing properties.
The aim of this work was to investigate the possibility of using plants for Hg removal
from a moderately contaminated industrial soil, increasing the metal’s bioaccessibility with
the use of these mobilizing agents.

Materials and Methods

Soil
Soil samples used in this work derived from an industrial site of a petrochemical plant
located in southern Italy.
Soil samples were air dried and ground to pass through a 2-mm sieve before laboratory
analysis. Soil pH was determined using a glass electrode in a soil/water ratio of 1:2.5,
cation exchange capacity (CEC) was determined using barium chloride (pH = 8.1), and
texture was measured by the pipette method (SSSA 1996).
The soil was also preliminarily characterized for fertility parameters: nitrogen (N),
phosphorous (P), potassium (K), and organic matter, according to the methods of soil
analysis (SSSA 1996).

Soil Extraction
To determine the most efficient additives to release Hg from soil in order to increase the
potential bioavailability of the metal, several extractions were carried out with extracting
solution as reported in Table 1. Extractions were run in triplicate in 50-mL polypropylene
centrifuge tubes. The mixtures of soil/extractant with a ratio 1:20 were shaken in a rotating
shaker overnight at 45 rotations per minute (rpm), and the supernatant that separated after
centrifugation at 15000 rpm for 15 min was analyzed for Hg content.

Table 1
Soil extractions and amounts of extractable mercury (mg kg−1 ) from the contaminated
soil (each value is the average of two replicates)

Extractant solution Abbreviation Reference Hg (mg kg−1 )

6.7 mM (NH4 )2 S2 O3 TS1 Moreno et al. (2004) 2.00 ± 0.4
13.5 mM (NH4 )2 S2 O3 TS2 4.96 ± 0.2
33.7 mM (NH4 )2 S2 O3 TS5 7.24 ± 0.2
0.27 M (NH4 )2 S2 O3 TS6 9.01 ± 0.3
0.11 M CH3 COOH AA Sanchez et al. (2005) 0.028 ± 0.002
1 mM H2 C2 O4 OA Slowey et al. (2005) 0.021 ± 0.003
1 mM C6 H8 O7 CA 0.018 ± 0.002
1 mM OA + 1 mM CA OA+CA 0.014 ± 0.004
(1:1 ratio)
100 mM KI, pH = 1.5 KI100 Wasay et al. (1995) 4.92 ± 0.3
1 mM KI, pH = 1.5 KI1 Wang (2004) 0.58 ± 0.1
2770 F. Pedron et al.

Microcosm Setup
After preliminary experiments with several species (data not reported), two plant species,
which showed the best growth on this soil, were selected for microcosm trials: B. juncea
var. scala and P. annua var. reptans. The trials were carried out in 250-mL pots by sowing
these plants on 200 g of soil per microcosm using about 0.3 and 0.1 g of seeds, respec-
tively. The soil used in microcosm experiments was prepared by eliminating the coarser
materials, accurately homogenized but without sieving to 2 mm, to obtain a sample more
representative of the real situation. Experiments were carried out in a growth chamber
in controlled conditions: 14 h of light, with a temperature of 24 ◦ C, and 10 h in dark
conditions at 19 ◦ C. Relative humidity was maintained at 70% (Pedron et al. 2009). As
treatments started, treated microcosms were separated from controls and placed under an
aspirator to avoid every possible type of contamination deriving from a volatilization of Hg
from treated soils, maintaining exactly the same conditions for controls and treated micro-
cosms. Mercury volatilization (measured by the Supervisor Office of Safety) was always
negligible. During the growing period, plants were watered daily.
Treatments with the most efficient Hg-mobilizing additives started 20 days after sow-
ing. The solutions were 0.27 M (NH4 )2 S2 O3 (pH = 5.0) (TS6) and 100 mM KI (pH = 1.5)
(KI100). A lower (1 mM) concentration of KI (KI1) was initially tested but did not influ-
ence the Hg removal, and this rate of addition was discarded even though it was suggested
in the literature (Wang 2004).
The solutions were added to microcosms by splitting the total dose, 10 mL in each
case, over 5 days to avoid or at least to minimize possible toxic effects on plant species
(Tassi et al. 2004), even if the solutions alone did not show phytotoxicity. Three replicates
for each treatment were prepared with controls (composite soil without additive solution)
and run simultaneously. Experiments lasted 40 days, and then plants were harvested.
Aerial parts were separated from the roots and washed with deionized water. The roots
were also washed in an ultrasound bath (Branson Sonifier 250 ultrasonic processor;
Branson, Danbury, Conn.) for 10 min to eliminate soil particles that could have remained
on root surfaces. Vegetal samples were left in a ventilated oven at a temperature of 40 ◦ C
until a constant weight was obtained. The dry mass of shoots and roots was gravimetrically
determined.

Mercury Analysis
Mercury concentration in soil, plant samples, and surnatants from extraction procedures
was determined by atomic absorption spectrophotometry with an Automatic Mercury
Analyzer (AMA 254, FKV, Bergamo, Italy). The analysis was performed directly on the
sample, both liquid and solid, by placing a known amount into a Ni boat, which entered
into the instrument. The analysis was based on Hg vapor produced during combustion and
decomposition phases. The entire process was performed under oxygen flux by thermal
decomposition, amalgamation, and atomic absorption spectrophotometry using the SW-
846 method 7473 (U.S. EPA 1998). The working condition of this instrument permits
reaching high values of sensitivity.

Quality Assurance and Quality Control

Quality assurance and quality control were performed by testing standard solution every 10
samples. Certified reference material was used to control the quality of analytical system.
 Mercury Phytoextraction 2771

The detection limit for Hg was 2 mg L−1 . The recovery of spiked samples ranged from 94
to 101% with a Relative Standard Deviation (RSD) of 1.91 of the mean.

Statistical Analysis
All statistical analysis was performed using Statistica version 6.0 (Statsoft, Inc., Tulsa,
Okla.). Treatment effects were analyzed using one-way analysis of variance (ANOVA).
Differences among means were compared, and a post hoc analysis of variance was
performed using the Tukey’s honestly significant differences test (P < 0.05).

Results and Discussion

Soil was characterized by the following parameters: pH 7.9, organic matter 1.6%, total N
0.06%, available phosphorus (P) 11.9 mg kg−1 , available potassium (K) 193 mg kg−1 , and
cation exchange capacity 20.6 cmol(+) kg−1 . The texture was sand 66.9%, clay 19.0%, and
silt 14.1%. Mercury was the only contaminant. The total Hg concentration was 14.8 mg
kg−1 . Fertility parameters were determined to evaluate if the conditions were suitable for
plant growth, and the results suggest that the N and P were sufficient for the short growing
period of microcosm experiments. No fertilization practice was executed.

Extractable Hg Concentrations
The process of phytoextraction is possible if Hg is present in soil in soluble forms, because
in this condition it is potentially available to plants. In the case of low solubility, plant
uptake can be enhanced by adding chemical agents to soil that can mobilize it. In the soil-
specific conditions, (NH4 )2 S2 O3 and KI were selected as the best agents to solubilize the
metal, leading to the formation of soluble salts and different kinds of complexes such as
2−
Hg–iodide complexes (HgI− 3 , HgI4 ) or Hg–thiosulfate complexes (NH4 [Hg(S2 O3 )3 ] ).
+

The degree of mobility depends on the charge of the complexes and the adsorbing surfaces
in the soil.
Recent studies (Moreno et al. 2004, 2005a, 2005b; Wang 2004) have highlighted
the positive effects of thioligands and KI solutions to increase Hg bioavailability for
plants; however, preliminary studies were conducted to determine whether other extrac-
tants were also able to mobilize the metal from this specific contaminated soil. Mercury
concentrations released in extracting solutions are reported in Table 1. The greatest
efficiency in extraction of Hg was obtained with TS and KI in the following order:
TS1 < KI100 = TS2 < TS5 < TS6. The Hg concentrations in these extracts reached
values of about 2, 5, and 7 mg kg−1 , respectively. The other reagents, AA, OA, CA, and
OA + CA, have extracted lower Hg concentrations from the soil with respect to TS and
KI100, with values that ranged from about 0.015 to 0.030 mg kg−1 .
These results showed that Hg solubility was not very high in the examined soil. Also
in other cases the solubility of Hg was very low both in sediments (Sahuquillo et al. 2003)
and soils (Boszke et al. 2008). Therefore, we needed to increase Hg concentration in the
mobile forms to promote the phytoextraction process by using mobilizing agents.

Microcosm Experiments
The aerial part biomass of plants, in the growth period of 40 days, is reported in Figure 1
for control and treated soils. In general, the increasing Hg uptake by plants produced
2772 F. Pedron et al.

200 Poa annua

Aerial part dry biomass (mg) DW

b b
Brassica juncea
150
a
100

50 b
a a

0
CT TS6 KI 100

Figure 1. Aerial dry biomass (mg) DW of P. annua and B. juncea grown in control (CT) and treated
soils (TS6, KI100). Bars indicate standard deviation of n = 3 replicates, and means with different
letters for the same plant are significantly different from each other (p < 0.05) according to the
Tukey test.

phytotoxic effects with significant growth reduction and has been reported in several plants
(Ampiah-Bonnet, Tyson, and Lanza 2007; Greger, Wang, and Neuschütz 2005). Also, in
our study, the yields were greater in the control microcosms; however, as shown in Figure 1,
different behaviors were obtained between the two plant species following the treatments.
Results showed that in the case of P. annua the decrease in dry biomass was quite similar
with each treatment of about 55% with respect to controls. For B. juncea, the yield was
35% lower than in controls after the KI100 addition, while no significant variation was
discovered after TS6 treatment. Phytovolatilization of Hg in our experiment was negligible
(measures performed by the Supervisor Office of Safety). Results are in accordance with
data of Greger, Wang, and Neuschütz (2005).
The mobilizing agents were added to microcosms by splitting the total dose over
five days (Tassi et al. 2004) to minimize any phytotoxic effect. Nonetheless, evident toxic
symptoms in plants treated with KI100 were observed. During the treatment, plant leaves
became yellow and then fell off. The root system also appeared damaged, being fragile and
dark. The plants died after the treatment. These effects were present in both plant species,
although B. juncea showed greater resistance. This could be ascribed to the different
tolerances of the two plants to the increased Hg uptake. Negative effects on plant growth
derived from KI must be taken into account; the dose used is too high for phytoremediation
because of the toxicity of KI at this concentration. As previously reported, a concentration
greater than 1 mM was not indicated for phytoremediation (Wang 2004), but it was used
tentatively to solubilize as much Hg as possible (Wasay, Arnfalk, and Tokunaga 1995).
Thiosulfate-treated plants showed lower toxicity symptoms probably because of the
fertilizing effects of (NH4 )2 S2 O3 , which promote plant health (Moreno et al. 2005a).
Addition of the mobilizing agents promoted Hg uptake by plants, both in the case of
B. juncea and P. annua, with respect to control microcosms (Figure 2).
In the controls, plants without any treatments, the greatest Hg concentration found in
the aerial part was about 1.5 mg kg−1 for B. juncea plants. In the root portion, the two plant
species showed different trends; Hg concentration was about 13 times greater in B. juncea
than in P. annua roots, in which the value was nearly 4 mg kg−1 .
The addition of a TS6 solution to soil promoted Hg uptake in the aerial part of the
plants, reaching Hg concentrations of 100 mg kg−1 for B. juncea and 140 mg kg−1 for P.
 Mercury Phytoextraction 2773

(A)
500
c
400
Hg (mg kg–1)
300

200 b
b b
100
a a
0

700 (B)
b
600 c
b
500
Hg (mg kg–1)

b
400
300
200
100 a
a
0
CT TS6 KI100 CT TS6 KI100

Poa annua Brassica juncea

Figure 2. Mercury concentrations (mg kg−1 ) in the aerial part (A) and roots (B) of P. annua and B.
juncea. Bars indicate standard deviation of n = 3 replicates, and means with different letters for the
same plant tissue are significantly different from each other (p < 0.05) according to the Tukey test.

annua, which were about 70 and 400 times, respectively, greater than control values. In
the case of the roots, the concentration values were greater than in the aerial parts, 480 and
560 mg kg−1 for B. juncea and P. annua, respectively.
Treatment with KI100 favored Hg uptake in aerial part of the plants, mainly in P.
annua where concentration values were about 380 mg kg−1 , 1100 times greater than in
the controls. In the case of B. juncea, Hg concentration in the aerial part of treated plants
increased to about 100 mg kg−1 , a value 70 times greater than that of the controls, similar to
results obtained with the TS6 treatment. Mercury concentrations in the roots of the plants
were around 450 and 350 mg kg−1 for P. annua and B. juncea, respectively, 120 and 7 times
greater than the control values. In the case of B. juncea, the differences between treated and
control microcosms were lower because of a greater efficiency of this plant species in the
control pots.
An important aspect to consider is the plant’s ability to translocate the contaminant
from the roots to the aerial part. This is expressed by the translocation factor (TF), the ratio
between Hg concentrations in aerial parts and in roots. The results, reported in Figure 3,
showed that in general treatments promoted the translocation of Hg to the aerial parts, with
the greater TF values in KI100-treated microcosms. The translocation was more evident in
the case of P. annua.
Compared with previous studies (Ampiah-Bonnet, Tyson, and Lanza 2007; Greger,
Wang, and Neuschütz 2005), results appear particularly interesting, because the ability of
plants to transport Hg to shoots is limited. In general, additives used to promote plant
uptake do not increase levels of Hg accumulation in shoots compared to roots.
2774 F. Pedron et al.

1.00

Translocation factor
0.80

0.60

0.40

0.20

0.00
CT TS6 KI 100 CT TS6 KI 100

Poa annua Brassica juncea

Figure 3. Translocation factor of P. annua and B. juncea grown in control (CT) and treated soils
(TS6, KI100). Bars indicate standard deviation of n = 3 replicates, and means with different letters
for the same plant tissue are significantly different from each other (p < 0.05) according to the
Tukey test.

20.0
c

15.0
b
µg

10.0
c

5.0
b

a a
0.0
CT TS6 KI 100 CT TS6 KI 100

Poa annua Brassica juncea

Figure 4. Total uptake (µg) of Hg in the aerial part of P. annua and B. juncea. Bars indicate standard
deviation of n = 3 replicates, and means with different letters for the same plant are significantly
different from each other (p < 0.05) according to the Tukey test.

The amount of Hg accumulated in plant tissues is the result of two dynamic pro-
cesses, metal uptake and transport, and biomass production, and can be expressed as “total
accumulation” (Jarrell and Beverly 1981). Data are reported in Figure 4.
In general, the treatments used favored the total accumulation of Hg in plant aerial
parts with respect to controls. In the case of P. annua, the increase was from 0.014 µg to
about 2.8 µg after TS6 treatment, which is more than 200 times the control value. The
results are in accordance with other findings in different Hg-contaminated soils (Moreno
et al. 2005a). Following KI100 addition, Hg amounts found in plant aerial tissues were
around 7.5 µg, nearly 560 times greater than the values found in control plants. The com-
parison between the two treatments showed that KI100 was the more efficient for P. annua,
increasing the total accumulation nearly three times with respect to that obtained with
TS6 solution.
 Mercury Phytoextraction 2775

The situation was the opposite for B. juncea. Best results were obtained with TS6 treat-
ment, reaching Hg accumulation in aerial part of plants that was about 1.5 times greater
than that obtained with KI100 solution. The values were 17.5 and 11.4 µg after TS6
and KI100 treatments, respectively. In both cases, there was an increase of Hg amounts
in the aerial part of B. juncea plants of about 70 (TS6) and 45 (KI100) times that of
the control.
As shown in Figure 4, the absolute value of “total accumulation” is low because of
the reduced amount of soil and short growing period. In these conditions, a comparison
between treatments and plant species efficiencies must be cautious; however, it is possible
to note that the increase in uptake of the Hg with respect to controls was greater in B.
juncea than in P. annua for all treatments.

Conclusions
The main goal of our study was to evaluate the use of plants to clean up Hg-
contaminated soil. Results showed that increasing the metal’s bioaccessibility with the
use of (NH4 )2 S2 O3 and KI promoted Hg uptake by plants, with respect to controls.
Further indications for potential use of plants for remediation can be drawn from the
values of the phytoextraction coefficient (PEC), defined by the ratio between the concen-
tration of Hg in the shoots and the initial concentration of Hg in soil. This coefficient is
generally used for evaluating metal uptake of plants after a short growing period and can
provide useful information for phytoremediation efficiency. A value between 0.5 and 60
is considered acceptable (Ampiah-Bonnet, Tyson, and Lanza 2007). The results obtained
showed that without any treatment the technology is not viable: PEC values were less than
0.1. After TS6 treatment, this coefficient raised to about 7.0 for B. juncea and to 9.4 for P.
annua. The KI treatment further increased the PEC value of P. annua to 25.6, while a value
similar to that obtained after TS6 treatment (7.0) was found for B. juncea. Data obtained
do support the potential for successfully applying the use of plants after addition of mobi-
lizing agents to reduce the Hg concentration in this contaminated soil, and the results could
be useful for remediation in similar industrial sites.

Acknowledgment
The authors thank Irene Rosellini for technical assistance. Work supported by Saipem tech-
nical experts Gianstefano Cecca and Leonardo Pagnotta. Thanks to Enipower (Rosario
Cigna e Giuseppe Marasco) for the financial aid in phytotechnology development.

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