Heavy Metals and Arsenic Phytoavailability Index in
Pioneer Plants from a Semipermanent Natural
Wetland
Juan Miguel G omez-Bernal ,a Esther Aurora Ruiz-Huerta,b Marıa Aurora Armienta Hern
a
Vıctor Manuel Luna-Pabello
a
Departamento de Biologıa, Facultad de Quımica, Universidad Nacional Autonoma de Mexico, 04510, Mexico;
gupi02@yahoo.com.mx (for correspondence)
b
Departamento de Recursos Naturales, Instituto de Geofısica, Universidad Nacional Autonoma de Mexico, 04510, Mexico
Published online 21 September 2017 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/ep.12759
The total concentration of Pb, Zn, Cu, Fe, Mn, and As in
mining-impacted soils and pioneer plants from a semi-
permanent natural wetland was determined by X-ray fluo-
rescence. Results showed that the maximum values in soil
were Fe > Zn > Pb > Mn > As > Cu and in plants were
Zn > Pb > As > Cu, and Mn and Fe were found in variable
concentrations. Bouteloa repens showed the highest translo-
cation factor (TF) for all heavy metals, and the highest phy-
toavailability index (PI) for Fe, Cu, As, and Mn. However,
Typha dominguensis was the plant species with the most ele-
vated bioconcentration factor (BCF) for Mn and Fe and PI
for Pb and Zn, while Cyperus manimae showed the maxi-
mum BCF for As, Pb, and Cu, and the highest PI for Mn. For
Eleocharis ovata the maximum BCF and PI were for Zn and
As, respectively. The PI indicates the availability of heavy
metals and As in the environment and their bioaccumula-
tion in plants. The plant species reported in this study are
pioneer plants that can easily become established due to their
environmental resilience and physiologic characteristics. This
study shows that B. repens and T. dominguensis are species
that translocate heavy metals and accumulate them in their
various organs, and therefore, these plants are suggested as
good candidates for phytostabilization in similar semi-
permanent natural wetlands. V C 2017 American Institute of
Chemical Engineers Environ Prog, 37: 980–988, 2018
Keywords: natural wetland, heavy metals, mining wastes,
translocation, bioconcentration
INTRODUCTION
Wetlands are transitional water ecosystems characterized
by the presence of water-tolerant plants, such as cattails,
sedges, and mosses [1,2]. Wetlands purify, recycle, and retain
nutrients, pollutants, and sediments through unique mecha-
nisms of adaptation that include redox transformations, vege-
table retention of pollutants, microbial degradation, and
sedimentation [3]. The impact of mine discharges containing
heavy metals and As is mainly due to all water used in and
resulting from the beneficiation process. Wastewater is often
poured around the mine and, therefore, can reach wetlands.
C 2017 American Institute of Chemical Engineers
V nguensis is emergent and rhizomatous, being palustrine or
980 May/June 2018 Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep
andez,b and
The effects of such wastewater are evidenced by the increase
of heavy-metal concentrations in sediments and by the
decrease in biota at the site, which reduces the ecosystem
productivity and becomes a potential risk to humans [4].
Treating and minimizing mine-waste leachates is challeng-
ing, mainly due to their variability in pollutants and their con-
tent, as well as their high potential to negatively impact the
adjacent aquatic systems. Mine-waste leachates carry particles
that are deposited in the sediments. These sediments may
retain toxic metals and metalloids in a stationary state or may
allow their translocation to the aerial parts of the plants. Thus,
wetlands are a major reservoir for these metals [5,6]. Vegetation
plays a key role in the performance of wetlands, as it contrib-
utes to reducing the pollution load through phytoextraction,
phytostabilization, transpiration, and rhizofiltration [7]. Vegeta-
tion increases the efficiency of evapotranspiration [8]. However,
plant species in wetlands differ in their ability to capture metals
in their roots and in the translocation of those metals to their
aerial parts [9]. Additionally, plants colonized in mine-tailing
soil and water have abnormal chemical and physical properties.
Only plants that have evolved through natural selection and
adapted to specialized environments can colonize such sites
[10]. Several pioneer plant species have been identified that
show successful establishment and colonization in mine-tailing
sites, for example, Leucaena leucopephala [11]. These pioneer
or colonizing plants bear special morpho-anatomical character-
istics that allow them to adapt and become established in envi-
ronmentally affected sites. They need to be resilient and grow
fast to be able to survive in the unfavorable conditions found
in this kind of disturbed habitat.
Eleocharis is a widely distributed genus of about 200 spe-
cies. It has been receiving attention because of the potential
use of several if its species in aquatic weed management and
in pollution abatement. Cyperus is a large genus of about
700 species, whose habitat is particularly in oak forests and
wetlands at elevations from about 2000 to 2700 m. Bouteloa
repens is a strong perennial plant with culms up to 60 cm
tall, and its habitat is usually hilly terrain on a wide variety
of soil types. It is present on sandy ocean shores near sea
level, to mountain slopes at elevations of 2500 m or higher,
and grows under moderate habitat disturbance. Typha domi-
Figure 1. Distribution of plant species in the semipermanent wetland close to the mining wastes “La Concha” in Taxco,
Mexico.
aquatic. Its growth height is up to 3–4 m, and it spreads rap-
idly by vegetative reproduction and generative reproduction.
The importance of this plant in wetland ecosystems is due to
the large amount of organic matter produced by decomposi-
tion [12]. It also grows in industrial wastewater lakes, which
indicates that the plant is resistant to pollution and associa-
tions in disturbed and eutrophic wetlands.
The contaminated area for the current study was chosen
based on previous studies performed in that mining site and
that have focused primarily on the geochemical behavior of
heavy metals (Pb, Zn, Cu, Mn, and Fe) and As [13–16]. This
study was carried out with the following aims: (1) to identify
plant species that develop naturally in a semi-permanent
wetland and (2) to assess the tolerance and accumulation of
heavy metals and As in plant tissues for further consideration
in phytostabilization in areas with similar characteristics.
MATERIAL AND METHODS
Geographic Delimitation
Plants were collected in a semi-permanent natural wet-
land (300 m2) located in Taxco de Alarcon, Mexico (Figure
1). Taxco is a municipality located in the Northern part of
the state of Guerrero, with an altitude of 2,600 m above sea
level (188 210 N, 998 470 W). The annual temperature varies
between 128C and 268C, and the range of annual precipita-
tion is 800–1500 mm [17]. La Concha tailing pond is located
north of the San Antonio mine (Figure 1) at 188320 22.2719100
N, 998380 9.053700 . It is an irregularly shaped deposit, 140-m
long, 50-m wide, and 10-m tall [18].
Taxonomic Determination
The collection method used was that proposed by Lot
and Chiang [19]. This method consists of collecting, pressing,
drying, making the taxonomic determination, labeling,
mounting, folding, and archiving. The species identification
was conducted by the Metropolitan Herbarium at the Univer-
sidad Aut
onoma Metropolitana-Iztapalapa (UAM-I). Speci-
mens were incorporated into the collection based on the
taxonomic criteria of Brummitt and Powell [20].
Determination of Heavy Metals and As
Soil Sampling
Composite samples were collected in the semipermanent
natural wetland at five distant points at depth ranges of 0–
35 cm. Samples contained a mixture of soil and mining waste
Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep
and were taken from the rhizosphere zone. The total con-
centrations of heavy metals and As were measured in these
samples using a NITON XL3t Thermo Fisher Scientific spec-
trometer, and the X-ray spectra were obtained with a Niton
software transfer data. The spectrometer was calibrated with
certified NIST standard reference material for heavy metals in
soils (Montana soil 2710 and 2711). Each sample concentra-
tion was measured in triplicate. As also was measured by X-
ray fluorescence, which is a technique already accepted by
the US Environmental Protection Agency to quantify As in
dry solid samples [21].
Plant Samplings
Plant samples were collected from the semipermanent
natural wetland at five sampling sites by collecting three
individual plants per site. Individual plants were divided to
perform two procedures: (1) an assay for heavy metals and
As content and (2) taxonomic identification. Plants were
washed in the laboratory with tap water, followed by three
rinses with deionized water (18 MX cm21, Milli-Q Millipore)
and one rinse with tri-distilled water. All plant samples
were carefully separated into leaves and roots and dried at
608C for 75 h. Dried plant samples were then crushed,
sieved (<325 lm), homogenized, and weighed. Then, the
chemical assays were performed by X-ray fluorescence
spectrometry. X-ray spectra were obtained from Niton soft-
ware transfer data. The spectrometer was calibrated with
certified NIST standard reference material for heavy metals
in plants (peach leaves, NIST 1547). Each assay was per-
formed in triplicate.
Translocation and Bioconcentration Factors
The values of the heavy metals and As concentrations
were used to estimate the translocation factor (TF) and the
bioconcentration factor (BCF). TF was defined as the average
of the heavy-metal or As concentration in leaves divided by
the heavy-metal concentration in the roots [15, [22,23]]. The
BCF was defined as the average of the heavy-metal or As
concentration in plant tissues divided by the heavy-metal or
As concentration in the soil [15, 23, [24]].
Concentration of the heavy metals or As in leaves
TF 5
Concentration of heavy metals or As in roots
Concentration of the heavy metals or As in plant tissues
BCF 5
Concentration of heavy metals or As in the soil
May/June 2018 981
Table 1. Concentrations of heavy metals and As (mg/kg) in various substrates and in sediments of the wetland close to “La
Concha” tailings in Taxco, Mexico.
Pb
Substrate mg/kg
Taxco wetland sediments. 7315.6
Average soil range [26] 2–300
Soil phytotoxic concentrations [26] 100–400
Concentrations in metalliferous soils [27] 3870–49,910
Mexican regulation [28] 400
Phytoavailability Index for Heavy Metals and As
The phytoavailability index (PI) for heavy metals and As
was determined by dividing the total concentration of heavy
metals or As in soil by the total concentration of heavy met-
als or As in plant tissues [25].
Concentration of the heavy metals or As in soil
PI 5
Concentration of heavy metals or As in the plant tissues
RESULTS
Taxonomic Determination
The collection of plants was made based on abundance,
and the four dominant species were identified in the wetland
in the following decreasing order of abundance: Cyperus
manimae (L.) Kuhn, Eleocharis ovata (Roth) Roem. & Schult,
Bouteloa repens (Kunth) Scribn. & Merr, and Typha domi-
nguensis Pers.
Metal and As Content in Soil
High concentrations of heavy metals and As were found
in the wetland soil samples: Pb (7315.6 mg kg21), Zn
(48029.0 mg kg21), Mn (3000.0 mg kg21), Cu (700.4
mg kg21), Fe (13.8%), and As (1407.3 mg kg21) (Table 1).
Metal and As Content in Plants
The concentrations of heavy metals and As in roots were as
follows: in C. manimae, Pb (13866.1 6 2081.7 mg kg21), Cu
(918.8 6 18.5 mg kg21), and As (5707.4 6 100.0 kg mg21); in T.
dominguensis, Mn (106000.0 6 9300.0 mg kg21) and Fe
(22.2% 6 17.8%); and in E. ovata, Zn (41972.6 6 2309.4
mg kg21) (Table 2). The concentrations of the heavy metals
and As in the leaves were as follows: in B. repens Pb
(16938.6 6 3491.9 mg kg21), Zn (48748.6 6 9931.8 mg kg21),
Cu (1071.4 6 153.2 mg kg21), Mn (15000.0 6 3000.0 mg kg21),
and Fe (31.4% 6 6.7%); and As was present in the highest con-
centration (2304.29 6 173.9 mg kg21) in C. manimae.
Translocation Factor and Bioconcentration Factor
The TF calculations for each species indicated that B. repens
has the best ability to translocate Pb (3.5), Zn (2.9), Cu (2.1),
Mn (4.8), Fe (6.5), and As (2.1) from the roots to the leaves
and that E. ovata showed the second-highest values for heavy
metals and As. A TF value very close to or greater than 1
means that metals are completely translocated from the root to
the leaves. The highest BCFs were obtained in C. manimae for
Pb (1.9), Cu (1.3) and As (4.1), in E. ovata for Zn (0.9), and in
T. dominguensis for Mn (29.9) and Fe (1.5). These values are
high and indicate accumulation of heavy metals and As, mainly
in C. manimae and E. ovata (Figure 3A).
Phytoavailability Index for Heavy Metals and As
The highest values for the PI were observed in T. domi-
nguensis for Pb (31), Zn (11.9), and As (1) and in B. repens
982 May/June 2018 Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep
Zn Cu As Mn Fe
%
48,029 700.4 1407.3 3000.0 13.8
1–900 2–250 0.1–40
70–400 60–125 0.5
109–70,480 52–50,900
22
for Cu (0.8), Mn (0.4), and Fe (1.6) (Figure 3B). The PI indi-
cates a high availability of heavy metals and As in the envi-
ronment depending on the species.
DISCUSSION
Taxonomic Determination
E. ovata (Roth) Roem. & Schult was identified in the ini-
tial part of the wetland in patches that interact with bryo-
phytes; B. repens (Kunth) Scribn. & Merr was located in the
middle of the semi-permanent natural wetland interacting
with bryophytes and E. ovata to a lesser extent; C. manimae
(L.) Kuhn was located at the end of the wetland in patches;
and T. dominguensis Pers. was located at the end with a
water presence. Some of these species of the genus Eleocha-
ris have been reported in other studies of wetlands in which
these plants grow on substrates with high concentrations of
heavy metals and As [32–35]. The genus Eleocharis includes
about 200 species that are distributed worldwide in aquatic
habitats and wetlands [36]. Several species of Eleocharis,
including E. acicularis, E. dulcis, and E. equisetina, have
been reported to colonize tailing ponds and impacted
streams, which explains the presence of E. ovata in the study
site. E. acicularis is an aquatic macrophyte that accumulates
various heavy metals from tailings and acid drainage; it has
also been reported to be a hyperaccumulator of Pb [32] and
to accumulate As, Cu, Fe, Mn, Ni, Sb and Zn [32] [37]. Simi-
larly, several studies have demonstrated the ability of Typha
species (T. latifolia, T. angustifolia) to tolerate several heavy
metals, such as Cd, Zn, and Pb [38,39], which explains the
presence of T. dominguensis in the wetland of the current
study.
A study by Yadav and Chandra [39] demonstrated the
accumulation of heavy metals in T. angustifolia and Coloca-
sia esculenta in a distillery that pollutes a natural wetland in
India. These plants are reported to have a potential to phy-
toremediate wastewater polluted with heavy metals (Fe, Mn,
Cr, Zn, Pb, Cu, Ni, and Cd). Chayapan et al. [40] reported
hydroponic experiments during 15 days with C. esculenta,
Cyperus malaccensis, and T. angustifolia in solutions with
various concentrations of Cd and Zn. They concluded that
only C. esculenta could be considered a hyperaccumulator
of Zn, and they found that T. angustifolia had a high uptake
of Cd and Zn, thus confirming that this plant is a good can-
didate to treat contaminated soil and sediments with Cd.
In the current study, it was observed that the plants and
their distribution at the site did not show apparent damage.
Accordingly, E. ovata, C. manimae, and B. repens showed
near-normal growth. Because of their own environmental
resiliency and the characteristics of the species, the families
Cyperaceae and Poaceae reported here are considered to be
a group of colonizing plants that show easy establishment in
an ecological environment.
Therefore, based on the observations in Taxco and previ-
ous studies, the feasibility of establishing this group of plants
in soil contaminated by mining waste sites is assessed. This
 group of plants does not require further studies regarding

22.2 6 17.8
31.4 6 6.7
3.3 6 0.1
10.5 6 0.8
3.2 6 0.2
5.3 6 0.2

4.8 6 0.4
0.4 6 0.2
factors for their introduction since these species can become

Fe
established, develop, and spread with normal appearance.

% Metal and As Content in Soils

To understand the mechanisms of the accumulation of
heavy metals and As in the semi-permanent natural wetland,
chemical determinations were carried out to study the rela-

15000.0 6 3000

106000.0 6 9300
tionship between soils and plant species. The concentrations
2000.0 6 200
6000.0 6 300
3000.0 6 200
5000.0 6 200

3000.0 6 200
5000.0 6 500
Table 2. Heavy metals and As concentrations (mg/kg) in roots and leaves of plants growing in a natural wetland close to “La Concha” tailings, N 5 3. 6DE.

of heavy metals and As in the studied soils were higher than

those reported as normal ranges for soil (Table 1). Gomez-

300†
Mn

Bernal et al. [15] measured the following concentrations of

heavy metals and As in soil samples from La Concha tailing
pond: Pb (19125.05 mg kg21), Zn (37994.35 mg kg21), Cu
(1039.51 mg kg21), Mn (15.84 mg kg21), Fe (19.15
mg kg21), and As (1827.60 mg kg21). Soils were found to be
within the range of metalliferous soils [27] with the following
concentrations: Pb (3.870 to 49.910 mg kg21), Zn (109 to
1387.3 6 1034.9
2304.3 6 173.9
5707.4 6 100.0

70.480 mg kg21), and Cu (52 to 50.900 mg kg21). Morton

1226.4 6 208.2
2234.9 6 152.8
2138.7 6 92.7
1005.8 6 91.1

0.01–5**
45.9 6 8.1

et al. [16] determined a range of 23.625–40.250 mg kg21 Zn

in the available fraction, indicating a high availability envi-
As

ronment. In this study, the concentration of Zn was found to

be higher than that reported by Morton et al. [16]. The maxi-
mum values allowed for wetland soils by Mexican Standard
NOM-147-SEMARNAT/SSA1–2004 were exceeded (Pb 5 400
ppm and As 5 22 ppm). Therefore, the plant distribution pat-
tern in the studied wetland possibly was influenced by these
1071.4 6 153.2

894.6 6 667.9

concentrations and the plant life cycle, since clonality pre-

918.8 6 18.5
248.2 6 20.6

308.4 6 20.8
530.7 6 20.0

504.1 6 40.2
116.7 6 25.5

5–25*

dominates in plants under stressful conditions, such as

nitrogen-poor soil, wet soils, and water bodies [41–43].
Cu

Metal and As Content in Plants

Plants reported here grow naturally in small patches
(10 m2). This is important because this growing pattern also
was observed in the studied semi-permanent wetland where
mining wastewater is discharged.
41972.6 6 2309.4
48748.6 6 9931.8

500–1500††
17014.8 6 2516.8
37863.8 6 1693.0
41705.5 6 1513.6

17008.1 6 1490.0

3801.7 6 1428.6

The highest concentrations of heavy metals and As in the

238.9 6 172.9

20–400*

plant roots were found in C. manimae for Pb (13866.1

mg kg21), Cu (918.8 mg kg21), and As (5707.4 mg kg21); in
Zn

E. ovata the highest concentration was for Zn (41972.6

mg kg21); and in T. dominguensis it was for Mn (106000.0
mg kg21) and Fe (22.2%). The largest accumulations of
heavy metals and As in leaves were found in B. repens for
Pb (16938.6 mg kg21), Zn (48748.6 mg kg21), Mn (15000.0
mg kg21), Cu (1071.4 mg kg21), and Fe (31.4%), and in C.
manimae, it was for As (2304.3 mg kg21) (Table 2). In gen-
13866.1 6 2081.7

16938.6 6 3491.9

eral, T. dominguensis, E. ovata, and C. manimae accumu-

4647.8 6 304.2

3954.7 6 251.7
7670.2 6 300.0

4825.6 6 226.7

195.0 6 140.7

lated more heavy metals and As in roots than in leaves.

40.7 6 5.7

0.1–5*

However, B. repens accumulated more heavy metals and As

Pb

in leaves than in roots. For C. manimae, the As concentra-

tion was much higher in roots and leaves than in the sedi-
mg/kg

ment. Finally, E. ovata showed a similar accumulation of Zn

in both roots and leaves. This is interesting because Zn was
the only element showing this behavior, even so because
this Zn concentration was lower than that measured in the
sediments (Table 2). This may be related to the exchange-
able fraction, which is very high in the near tailing ponds,
organ
Plant

Leaves

Leaves

Leaves

Leaves

and the plant accumulates Zn without restriction due to this

Root

Root

Root

Root

high availability [16]. Ricachenevsky et al. [44] found that Zn

Phytotoxic concentrations

may become toxic at high concentrations in the soil, and this

study discovered that the concentration greatly exceeded the
phytotoxic concentration (Table 2).
Plant normal range

Ha et al. [32] found that E. acicularis accumulated Zn

T. dominguensis

(44.0–73.5 mg kg21), Cu (14.4–20.5 mg kg21), and As (2.67–

6.44 mg kg21) in 10 days under laboratory conditions. They
C. manimae

concluded that E. acicularis easily adapts and grows in Cu-,

B. repens
E. ovata

Zn-, and As-contaminated environments and that it is con-

Specie

[31].
**[29].
[30].
*[27].

trollable. Ha et al. [33] found that high concentrations of Pb

(1120 mg kg21) in the aerial parts of E. acicularis grown in
††
†

Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep May/June 2018 983

Figure 2. Arsenic and heavy metals concentrations
(root 1 leaves) in four plant species growing in the semiper-
manent wetland close to “La Concha” tailings, Taxco,
Mexico.
water containing 2.0 mg L21 Pb and 1.0 mg L21 Cu accumu-
lated 575 mg kg21 Cu. Sakakibara et al. [45] found that E.
acicularis accumulated 20,200 mg kg21 Cu 2 months after
transplantation of specimens to an abandoned acid drainage
site in Japan.
Ha et al. [33] found high concentrations of Zn (213
mg kg21) in the aerial parts of E. acicularis growing in a
solution containing 1.0 mg L21 Zn. However, this study
found that E. ovata accumulated Zn in concentrations of
41,705.5 mg kg21 in leaves, and 41,972.6 mg kg21 in roots
(Table 2). These values are higher than that reported by
Sakakibara et al. [45] of 13,700 mg kg21 Zn in 2 months after
transplantation in an abandoned acid drainage site. These
studies show the adaptation of the species and their potential
to accumulate Zn.
E. equisetina has been reported to develop in acid drain-
age in Queensland, Australia [46]. This plant is known to be
a fast-growing macrophyte with the ability to capture signifi-
cant amounts of nitrogen and phosphorus. E. equisetina
grew at pH 2.4, and apparently, the growth of other wetland
plants was inhibited by the high acidity and the content of
heavy metals and metalloids from leached tailings [34]. How-
ever, Lottermoser and Ashley [34] found that E. equisetina
excludes most heavy metals and metalloids, except Mn,
which was present in high concentrations (735 mg kg21 in
the aerial part and 550 mg kg21 in the roots). This plant has
colonized Jumna tailings in a mining area of Queensland,
Australia, since 1980 in a natural way in two small patches
(50 and 200 m2). A similar patchy colonization behavior was
observed in the current study (Figure 1).
For a plant to be established as a hyperaccumulator, it must
meet several requirements. In the case of Zn, the plant must
accumulate 10,000 mg kg21 [47]. The results of this study show
that C. manimae and B. repens meet that requirement and are
Zn hyperaccumulators; however, further experiments should be
performed to assure this classification.
The metal distribution pattern among the plant organs
was observed and found to be, in decreasing order, root > r-
hizome > leaves > stems, as reported for other wetland plants
species in heavy–metal-impacted estuaries (Phragmites aus-
tralis, Typha capensis, and Spartina maritima) and coasts
(Cymodocea nodosa) by Phillips et al. [48] and Bonanno
et al. [49]. The results of this study demonstrate that the main
accumulation is found in roots, which is precisely the organ
where there are not many metabolic pathways that could
affect plant development.
In Figure 2 shows such a large accumulation of Zn in C.
manimae, E. ovata, and B. repens. Zn is an important ele-
ment for metabolic functions, plant growth, and develop-
ment [50]. However, high contents of Zn can affect the
984 May/June 2018 Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep
normal growth of plants by decreasing the leaf area,
influencing the synthesis of chlorophyll, and, thus, inhibiting
the photosynthesis and producing alterations of the chloro-
plast structure. An excess of Zn also may cause the inhibition
of enzymes in the Calvin cycle, such as RuDP carboxylase/
oxygenase, PEP carboxylase, fructose-6-phosphate dikinase,
among others [51]. Gisbert et al. [52] found that an excess of
Zn in the substrate induces a significant reduction in biomass
production in Brassica plants that develop in soils contami-
nated by Zn compared to the control plants; they also found
that this metal accumulates more in stems, leaves, and
inflorescence.
Translocation Factor and Bioconcentration Factor
To assess the ability of plants to translocate metals from
the roots to the aerial part, the TF was calculated. Plants
accumulating heavy metals are characterized by a TF greater
than 1 [22]. B. repens showed the highest TFs for Pb (3.5),
Zn (2.9), Cu (2.1), Mn (4.8), Fe (6.5), and As (2.1). A value
of 1 for Zn also was determined in E. ovata and 2.9 in B.
repens, possibly indicating the accumulation of Zn (Figure
3A). Usually, only a small amount of Zn is taken from the
roots to accumulate it in the aerial part [53]. It is important to
note that both B. repens and E. ovata were the plants with
the highest translocation of heavy metals and As from the
roots to the leaves. Figure 3A shows very high TFs in B.
repens for the following elements in decreasing order:
Fe > Mn > Pb > Zn > As > Cu. This may be due to their com-
plex root systems, as they are pioneer species established in
sites with a natural or anthropogenic disturbance in areas
with low organic matter.
BFs were higher in C. manimae for As, Pb, and Cu. This
is relevant since Pb and As are nonessential elements. T.
dominguensis showed the highest BCF for Mn, Fe, and Cu.
E. ovata showed the highest BCF for Zn (Figure 3B), but it
was also high in C. manimae and B. repens. These results
reflect the availability of Zn in the substrate reported by Mor-
ton et al. [16] for the La Concha tailing pond of 32.2–39.8%
from a total concentration of 23,625–40,250 mg kg21 in the
available fraction, indicating a high environmental availability
of Zn.
Ha et al. [33] determined a high BCF for Pb (840), Cu
(520), and Zn (154) in E. acicularis grown in 1.0 mg L21
solution of Pb, Cu, and Zn. It is important to consider that,
in the case of As, the TF and BCF behaved differently among
plants. The first plant in contact with mine wastewater was
E. ovata, which had a BCF 5 1.6 for As, while C. manimae
had the highest, with BCF 5 4.1 for As. However, when com-
pared with the TF, the highest value for As was observed in
B. repens (2.1) and the lowest in T. dominguensis (0.03) (Fig-
ure 3B). Therefore, a combination of plant groups Cypera-
ceae and Poaceae might be a good alternative for
phytostabilization of heavy metals and As, thereby control-
ling them from spreading in the environment and preventing
their translocation into the food chain. It is important to con-
sider that As is a highly polluting metalloid, and among the
studied species, C. manimae was found to have the highest
value of BCF (4.1) (Figure 4). The results related to the cap-
ture of heavy metals from sediments to plants (BCF) and
their subsequent translocation (TF) indicate significant differ-
ences among the studied plant species and the studied ele-
ments, as also was reported by Bonanno et al. [49].
Natural wetlands are very complex environments. How-
ever, it is known that plants add a high As-retention capacity
to the wetland through various physicochemical mecha-
nisms, such as adsorption and complexation [54–56]. This
precipitation and immobilization of As are affected by the
chemical composition of the soil–root interface, by the oxi-
dation2reduction conditions created by reactions in the soils
Figure 3. Graphical representation of transference factors (TF), bioconcentration factors, and phytoavailability index (PI) in
studied plants.

Figure 4. Translocation (TF) and bioconcentration (BCF) factors in four plants species (C. manimae, T. dominguensis, B.
repens, and E. ovata) growing in the semi-permanent wetland.

caused by the presence of microorganisms, and by the pres-
ence of various mineral oxides [57]. Importantly, the accumu-
lation of As in B. repens indicates the trapping of the metal
on the substrate through rhizodeposition [58] (Figure 5b) and
its translocation in a small rate to the aerial parts. This low
translocation rate could be due to sequestering of heavy met-
als and As in the vacuole of the root cells, which may occur
as a natural response to toxic effects caused by metals [59]
(Figure 5a).
In turn, the plant species differ in the accumulation pat-
tern of heavy metals in the vegetative parts, which almost
always follows this decreasing order: roots > stems> leaves>
flowers [23, [60]]. However, this is not a set pattern, as it also
depends on the growth conditions and their abiotic
environment.
The expression of the accumulation of heavy metals and
As in different plant organs varies among metals. For exam-
ple, toxicity caused by Zn results in a reduced root elonga-
tion and chlorosis in young leaves, caused by a deficiency of
Fe21 [61]. Zn absorption is determined by a group of carriers
belonging to the ZIP family, which can be located in the
plasma membrane [62].

Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep May/June 2018 985
Figure 5. Processes of translocation and bioconcentration of heavy metals and arsenic.
However, there are plants that have no physical damage,
possibly because they have developed certain biochemical
mechanisms that allow them to isolate the toxicity of heavy
metals, which could be their deposition in the cell wall,
group (ASH) on the edge of the cytoplasm, cellular compart-
ments in isolation, complexation with organic acids, phenols,
and other organic compounds in the vacuole [15, [63,64]].
Phytoavailability Index for Heavy Metals and As
The PI for heavy metals and As was high in T. domi-
nguensis for Pb (31), Zn (11.9), and As (1). This indicates
high phytoavailability elements for the plant, which involves
their accumulation and translocation to the studied organs.
B. repens also had a high PI for Fe (1.6), Cu (0.8), and Mn
(0.4) (Figure 3C). B. repens and E. ovata showed the same
value for As phytoavailability, and B. repens and C. mani-
mae for Mn. These PI values indicate a high availability of
heavy metals and As in the environment, which depends on
the plant species, the activity and speciation of heavy metals
in the soil, and other plant genotypic variations in connec-
tion with capturing heavy metals or being resilient to them,
the interaction in the plant–rhizosphere–soil complex, among
others. Nawab et al. [65] found that native plant species can
be used to recover soils that are contaminated by the accu-
mulation of high concentrations of heavy metals.
These results show that the physical and chemical charac-
teristics do not prevent the translocation of heavy metals and
As to plants growing in sediments with high concentrations
of contaminants. Additionally, the compartmentalization strat-
egies are common in wetland plant species, and basically,
the main objective is to store high concentrations of heavy
metals in the underground organs (roots and rhizomes) as a
defense mechanism to protect the plant against the toxic
effects of those heavy metals on photosynthesis [48,49].
CONCLUSIONS
Few studies have been performed on semi-permanent
wetlands plants due to seasonality and species loss. How-
ever, the species reported here are characterized by their
permanence on the site throughout the year (dry and wet
seasons), which makes them relevant to deepening the
knowledge on their physiological and biochemical metal-
resilient mechanisms and to assessing their potential to be
986 May/June 2018 Environmental Progress & Sustainable Energy (Vol.37, No.3) DOI 10.1002/ep
cultivated in these habitats. This resilience was notorious in
B. repens, given the high values of the TFs for Pb, Zn, Cu,
As, Mn, and Fe, the BCFs for Zn, Cu, Mn, and Fe, as well as
the PIs for Cu, Mn, and Fe.
The information generated in this research could be used
to promote the formation of aquatic communities and wet-
lands with B. repens, E. ovata, C. manimae, and T. domi-
nguensis for the phytostabilization of heavy metals and As,
and somehow prevent contaminants from spreading to the
environment and avoid their transfer to the local food chain.
This study demonstrates the importance of continuing the
research on pioneer plants established in mine-tailing con-
taminated wetlands that may be used for contaminant-
removing purposes.
ACKNOWLEDGMENTS
Dr. Gomez-Bernal appreciates the postdoctoral fellowship
at the Facultad de Quımica, UNAM, granted by the Director-
ate General of the Academic Staff (DGAPA) of the UNAM for
the development of this research, which was funded by PAIP
50009111 granted to VMLP by the Facultad de Quımica,
UNAM, and to Luciano Hernandez G omez, MSc, for his tech-
nical support in processing the samples.
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