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Translocation, accumulation and bioindication

of trace elements in wetland plants

Article in Science of The Total Environment · March 2018

DOI: 10.1016/j.scitotenv.2018.03.039

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 Science of the Total Environment 631–632 (2018) 252–261

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Translocation, accumulation and bioindication of trace elements in

wetland plants
Giuseppe Bonanno a,⁎, Jan Vymazal b, Giuseppe Luigi Cirelli c
a
Department of Biological, Geological and Environmental Sciences, University of Catania, Via Longo 19, 95125 Catania, Italy
b
Czech University of Life Sciences Prague, Faculty of Environmental Sciences, Kamýcká 129, 165 21 Praha 6, Czech Republic
c
Department of Agriculture, Nutrition and Environment, University of Catania, Via Santa Sofia 100, 95123 Catania, Italy

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

• Capacity of trace element accumulation

is independent of plant life forms.
• Translocation from sediment to roots is
mainly species- and element-specific.
• Translocation across internal tissues is
mainly species-specific.
• Wetland plants are potentially suitable
for the phytostabilization of trace
elements.

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

Article history: This study aimed to shed further light on the capacity of macrophytes to translocate, accumulate and bioindicate
Received 11 December 2017 the levels of trace elements present in contaminated water and sediments. Specifically, this study aimed to find
Received in revised form 4 March 2018 evidence whether translocation, accumulation and bioindication are dependent on the kind of trace element and
Accepted 4 March 2018
plant species. To investigate the correlation between trace elements in plants and in the environment, the con-
Available online xxxx
centrations of As, Cd, Cr, Cu, Hg, Mn, Ni, Pb, and Zn were analyzed in twenty different wetland plants, and in
Editor: Charlotte Poschenrieder water and sediments from a wetland area affected by urban and industrial pollutants. Results showed that wet-
land plants share some common characteristics such as high tolerance to toxic element levels, capacity of
Keywords: phytostabilization and different element concentrations in the various organs. Moreover, element translocation
Environmental pollution from sediments to roots seems more influenced by the kind of plant species and trace element, whereas translo-
Macrophytes cation across the various organs seems mainly species-specific. No clear patterns of trace element translocation
Trace elements were identified according to plant life forms.
Element mobility © 2018 Elsevier B.V. All rights reserved.
Phytoremediation
Bioindicators

1. Introduction
Plant species play an important function in wetland geochemistry
because they are the main living collectors and transporters of trace
⁎ Corresponding author.
E-mail address: bonanno.giuseppe@unict.it (G. Bonanno).
elements through active and passive absorption (Bose et al., 2008;
Vodyanitskii and Shoba, 2015). Wetland plants can accumulate high
levels of trace elements from water and sediments thanks to their
well-developed root system, tolerance to toxicity, highly productive
biomass, and stationary nature (Milošković et al., 2013; Rezania et al.,
2016). In particular, wetlands are vulnerable to trace element inputs,
and the impact of element pollution is of great concern for the

https://doi.org/10.1016/j.scitotenv.2018.03.039
0048-9697/© 2018 Elsevier B.V. All rights reserved.
 G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261
ecosystem services affected (Mitsch and Gosselink, 2007; Bonanno,
2014; Bonanno and Vymazal, 2017). The consequences of high levels
of trace elements in wetlands are also difficult to investigate for the
complex behavior and interactions of such elements in aquatic ecosys-
tems (Verhoeven et al., 2006). Trace elements may affect the fragile eco-
logical stability of wetlands, whose fundamental role in nutrient cycling
and pollution control is widely recognized (Everard, 2017). Investigat-
ing the relationship between trace elements in water/sediments and
plant species is thus of the utmost importance to shed more light on
those processes of element translocation at the interface of plant organ-
isms and abiotic components.
Chemical contamination of water and soil resources is an ever-
increasing issue in most ecosystems around the world (Szyczewski
et al., 2009; Charlesworth et al., 2011; Bonanno and Orlando-Bonaca,
2018). Trace element contamination can be due to both natural geo-
chemical processes (e.g., weathering of ultramafic rocks), and human
activities (e.g., mining, smelting, combustion of fossil fuels, utilization
of fertilizers and pesticides, etc.) (Kabata-Pendias and Mukherjee,
2007; Dhote and Dixit, 2009; Bonanno and Pavone, 2015). Because of
their accumulative and non-biodegradable nature, trace elements are
potentially hazardous to natural ecosystems, and thus to all living or-
ganisms (Tchounwou et al., 2012). High levels of trace elements may in-
hibit life processes, and are particularly dangerous in aquatic
ecosystems where, once accumulated in sediments, they begin to
move up the food web, and biomagnify at higher trophic levels, ulti-
mately determining several chronic disorders in humans and animals
(Gall et al., 2015). Some elements, however, act as important
micronutrients for plants (e.g. Cu, Mn, Zn), even though such elements
may have also toxic effects at higher concentrations (Babula et al., 2008;
Kabata-Pendias, 2011). In turn, other elements (e.g., As, Cd, Cr, Hg, and
Pb), have no known biological roles and can prove highly toxic to organ-
isms even at low concentrations (Nagajyoti et al., 2010).
This study aimed to shed further light on the capacity of wetland
plants to translocate, accumulate and bioindicate trace elements in
water and sediments under toxic conditions in the field. To investigate
the relationship between trace elements in plants and surrounding en-
vironment, the concentrations of As, Cd, Cr, Cu, Hg, Mn, Ni, Pb, and Zn
were analyzed in twenty different plant species growing in a wetland
area affected by urban and industrial polluting inputs. These elements
include fundamental micronutrients (e.g. Cu, Zn) and toxic elements ac-
cording to the Italian Decree 260/2010. To date, relatively few studies
have investigated the translocation processes of trace elements in
large plant communities (e.g. Teuchies et al., 2013). The capacity of ele-
ment uptake varies indeed among plants (Bothe and Słomka, 2017), and
conducting a comparative analysis among several different species can
contribute to better understand the dynamics of trace element mobility
in wetland ecosystems. This study, in particular, aimed to identify com-
mon patterns of trace element translocation, but also to find further ev-
idence that translocation and bioindication of trace elements are mainly
species- and element-specific processes. This study aimed also to cor-
roborate previous findings on the capacity of wetland plants to tolerate
highly toxic levels of trace elements, and to phytoremediate contami-
nated sites.
2. Materials and methods
2.1. Study area
The study area was a coastal wetland (c. 50 ha) located on the out-
skirts of the town of Catania (Italy), (Fig. 1; 37°29′17.01′′N; 15°05′
16.25′′E). Catania has a total population of 315,000 inhabitants, which
reach 800,000 people with the whole metropolitan area. Specifically,
the study area is the estuary of a 6-km watercourse that marks the
southern border of the town, and was channelized to collect the munic-
ipal wastewaters from Catania. However, the quality of the water and
related sediments is significantly affected by untreated discharges of
253
domestic and industrial origins, which make this area highly contami-
nated. Other polluting sources included road run-off and illegal waste
dumping. The annual flow range is 0.50–2.0 m3/s, whereas annual rain-
fall and temperature are 600 mm and 18.0 °C, respectively. This wetland
is subjected to continuous polluting inputs, and is characterized by lux-
uriant aquatic and semi-aquatic vegetation. The control area was se-
lected within a nature reserve located 15 km south of the study area
(37°24′00.81′′N; 15°05′23.34′′E). The levels of trace elements detected
in plants from the control area (data not shown) were compared with
the levels of concentrations analyzed in the study area (see Table 8, let-
ter “K”). The control area hosted the same plant communities found in
the study area.
2.2. Sampling
A total of 20 different plant species was collected in the study area,
according to different life forms (Table 1). This implied the collection
of species with different ecology (e.g. semiaquatic vs permanently sub-
merged), biomass size, morphology and root systems (rhizomatous vs
free-floating). The rate of uptake and accumulation is age-dependent
in plant species (Kabata-Pendias, 2011). Specifically, with plant aging,
sensitivity to trace elements increases but is more related to the
functioning of photosynthetic tissues than to growth parameters
(Skórzyńska-Polit and Baszyński, 1997). We sampled only mature
plant individuals to neglect possible differences, due to age, in uptake
and accumulation of trace elements among the different studied spe-
cies. To reduce the potential action of environmental factors that may
influence the uptake of trace elements, we also selected sampling
plots with homogeneous environmental conditions (e.g. no recent
rains or floods, sampling on sunny and not windy days, absence of
waste). Collection of water, sediment and plant samples followed the
general protocols reported in Bonanno and Cirelli (2017). Sampling
was conducted in two months, April and October, and in two years,
2015 and 2016. Five sampling plots per each different species were ran-
domly selected within an area of 1000 m × 500 m. The average sampling
plot was a quadrate of 2 m × 2 m, and contained at least 10 different in-
dividuals of the same species to be collected. In each sampling plot, four
mature plant individuals of a given species, four samples of sediments
and four of water (1.0 L each) were collected. The plant individuals of
all species were delicately and wholly uprooted with stainless steel
tools, cleaned with linen cloths to remove extraneous materials (e.g.
gross ground particles), and put in sterilized plastic bags. Sediment sam-
ples were collected from the top 30 cm of the upper layer through a
Plexiglas corer (internal diameter 10 cm), and put in 1.0-L polyethylene
bottles. Water samples were collected within a radius of 0.25–0.50 m
from each collected plant individual, through 1.0-L sterilized glass bot-
tles, and at a variable depth of 0.20–0.50 m from the bottom to the
water surface. In total, we collected 400 different samples (observa-
tions) per each study month and year. All collected samples were gath-
ered in PVC containers and kept at 3 ± 1 °C until laboratory analysis.
Although the levels of some toxic elements were higher than the legal
limits, no collected plant specimen showed symptoms of toxicity (e.g.
impaired growth).
2.3. Chemical analysis
This study analyzed the concentrations of the trace elements As, Cd,
Cr, Cu, Hg, Mn, Ni, Pb and Zn in water, sediments and plant organs of the
studied species. Chemical analyses followed the procedures as reported
in Bonanno and Cirelli (2017). Once in the laboratory, plant samples
were first washed in running tap water to remove surface contamina-
tion, and then rinsed with bidistilled water to remove any further resid-
ual material on the surface. After that, plant samples were dissected into
roots, stems and leaves, and put in a refrigerator at 4 °C until chemical
processing. In case of rhizomatous species, roots and rhizomes were
treated together, and called “roots”. The weight of each dissected
254 G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261

Fig. 1. Study area: sampling plots were randomly selected within the areas of the yellow rectangles. (For interpretation of the references to colour in this figure legend, the reader is
referred to the web version of this article.)

organ ranged between 1.0 and 2.0 kg. Plant organs and sediments were
than dried to constant weight at ambient temperature. After drying,
plant samples were homogenized in an agate mortar, whereas sedi-
ments were passed through a 1.0 mm diameter sieve. The homogenous
plant powder and sieved sediments were then weighed at 0.10 ± 0.05 g,
and oven-digested at 90 °C overnight (microwave oven Mars 6, CEM
Corporation) in an acid solution (H2O2/HNO3, 2:3 ratio; Carlo Erba). Re-
garding water, samples were acidified with 63% HNO3 to pH ≤ 2, before
filtering through a 2.0 μm filter paper (Whatman® GF/A glass microfi-
ber filters). Once the digestion was complete, the solid residue of plant
PerkinElmer® AAnalystTM 400 AA Spectrometer). Quality control was
carried out through the stability of instrumental recalibration and
analytical blanks. The instruments were periodically checked against
the low level standards (once every five samples), and recalibrated
either when signs of drift were detected or after every 5 samples. The
Table 2
Levels of trace elements in the waters of the study area [mean values ± SD μg L−1], and
legal concentration limits (Italian Decree 260/2010).

and sediment samples was separated through centrifugation before Elements April 2015 April 2016 October 2015 October 2016 Legal limits
being passed through a 2.0 μm filter paper. Supernatants were finally di-
As 10.6 ± 1.87 8.67 ± 0.76 12.4 ± 2.21 11.9 ± 1.29 10.0
luted with ultrapure Milli-Q water to a final volume of 25 mL, and sub- Cd 0.65 ± 0.07 0.54 ± 0.06 0.78 ± 0.09 0.71 ± 0.09 –
jected to chemical analysis via ICP-MS (Cd, Cr, Cu, Mn, Ni, Pb, Zn), and Cr 4.78 ± 0.45 5.82 ± 0.49 4.89 ± 0.51 6.56 ± 0.60 7.00
FAAS (As and Hg) (respectively through PerkinElmer Elan® 6000, and Cu 24.8 ± 3.78 30.2 ± 4.56 18.9 ± 2.78 27.8 ± 4.03 –
Hg 0.26 ± 0.02 0.18 ± 0.02 0.23 ± 0.02 0.27 ± 0.03 0.06
Mn 0.68 ± 0.09 0.49 ± 0.06 0.56 ± 0.06 0.61 ± 0.08 –
Ni 14.8 ± 3.23 17.5 ± 3.45 16.9 ± 2.89 18.4 ± 3.67 20.0
Table 1 Pb 10.5 ± 1.56 8.93 ± 1.12 9.96 ± 1.89 8.67 ± 0.98 7.20
Life forms of the studied wetland plant species. Zn 4.78 ± 0.61 5.60 ± 0.72 4.90 ± 0.55 6.21 ± 0.69 –

Note: no statistical differences in concentrations were found in the four periods for each
Name Life form
element (one-way ANOVA, p b 0.05); N = 400 observations in total per each study
Alisma plantago-aquatica Rooted hydrophyte month and year.
Apium nodiflorum Rooted hydrophyte
Arundo donax Rhizomatous geophyte
Bolboschoenus maritimus Rhizomatous helophyte Table 3
Carex cuprina Tufty hemicryptophyte Levels of trace elements in the sediments of the study area [mean values ± SD mg kg−1],
Cyperus longus Rhizomatous helophyte and legal concentration limits (Italian Decree 260/2010).
Eichhornia crassipes Free-floating hydrophyte
Elements April 2015 April 2016 October 2015 October 2016 Legal limits
Epilobium hirsutum Scaped hemicryptophyte
Equisetum arvense Rhizomatous geophyte As 13.6 ± 2.02 10.5 ± 1.64 9.69 ± 1.90 11.8 ± 2.21 12.0
Juncus acutus Tufty hemicryptophyte Cd 0.96 ± 0.12 0.69 ± 0.08 0.75 ± 0.08 0.64 ± 0.08 0.30
Juncus maritimus Rhizomatous geophyte Cr 40.9 ± 6.74 35.8 ± 4.65 42.8 ± 6.89 40.8 ± 5.32 50.0
Lemna minor Free-floating hydrophyte Cu 145 ± 20.9 129 ± 18.8 138 ± 15.9 112 ± 16.9 –
Lemna gibba Free-floating hydrophyte Hg 0.55 ± 0.06 0.62 ± 0.08 0.59 ± 0.07 0.47 ± 0.06 0.30
Nasturtium officinale Scaped hemicryptophyte Mn 1100 ± 123 1059 ± 155 970 ± 108 1045 ± 198 –
Paspalum paspaloides Rhizomatous geophyte Ni 35.8 ± 5.78 40.7 ± 3.78 43.9 ± 5.02 38.9 ± 5.89 30.0
Phragmites australis Rhizomatous helophyte Pb 59.0 ± 6.78 65.8 ± 7.78 62.8 ± 7.54 67.9 ± 6.89 30.0
Typha angustifolia Rhizomatous helophyte Zn 389 ± 44.5 410 ± 32.9 356 ± 35.8 315 ± 28.0 –
Typha domingensis Rhizomatous helophyte
Note: no statistical differences in concentrations were found in the four periods for each
Typha latifolia Rhizomatous helophyte
element (one-way ANOVA, p b 0.05); N = 400 observations in total per each study
Veronica anagallis-aquatica Scaped hemicryptophyte
month and year.
 G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261 255

Table 4
Values of the bioconcentration factor per element in the studied species.

Name As Cd Cr Cu Hg Mn Ni Pb Zn Mean

Alisma plantago-aquatica 0.04 0.18 0.01 0.03 0.18 0.04 0.03 0.03 0.08 0.07
Apium nodiflorum 0.03 0.13 0.01 0.02 0.07 0.01 0.02 0.01 0.02 0.04
Arundo donax 0.03 0.13 0.03 0.04 0.45 0.02 0.08 0.02 0.02 0.09
Bolboschoenus maritimus 0.16 1.38 0.08 0.15 1.11 0.25 0.08 0.11 0.30 0.40
Carex cuprina 0.13 1.31 0.06 0.13 0.80 0.09 0.05 0.07 0.24 0.32
Cyperus longus 0.23 1.43 0.08 0.17 1.16 0.37 0.11 0.10 0.26 0.43
Eichhornia crassipes 0.25 2.04 0.10 0.15 2.41 0.40 0.09 0.12 0.30 0.65
Epilobium hirsutum 0.04 0.37 0.01 0.02 0.18 0.01 0.03 0.01 0.03 0.08
Equisetum arvense 0.05 0.46 0.01 0.06 0.27 0.06 0.07 0.04 0.18 0.13
Juncus acutus 0.16 1.25 0.06 0.12 1.16 0.10 0.12 0.06 0.20 0.36
Juncus maritimus 0.17 1.78 0.07 0.17 1.52 0.15 0.09 0.10 0.23 0.48
Lemna minor 0.16 0.55 0.08 0.11 1.21 0.21 0.08 0.10 0.22 0.30
Lemna gibba 0.13 0.46 0.06 0.08 0.98 0.18 0.04 0.08 0.18 0.24
Nasturtium officinale 0.02 0.09 0.01 0.02 0.05 0.01 0.02 0.01 0.02 0.03
Paspalum paspaloides 0.02 0.21 0.01 0.03 0.09 0.01 0.02 0.02 0.03 0.05
Phragmites australis 0.25 1.64 0.09 0.20 1.52 0.42 0.11 0.13 0.37 0.53
Typha angustifolia 0.15 1.32 0.05 0.12 1.04 0.19 0.11 0.10 0.26 0.37
Typha domingensis 0.18 1.38 0.08 0.14 1.29 0.22 0.14 0.09 0.28 0.42
Typha latifolia 0.23 1.47 0.06 0.10 1.48 0.20 0.13 0.08 0.30 0.45
Veronica anagallis-aquatica 0.06 0.34 0.01 0.03 0.31 0.05 0.06 0.06 0.12 0.12
Mean 0.12 0.90 0.05 0.10 0.86 0.15 0.08 0.07 0.18

validity and precision of the analytical procedures were assessed
through the standard reference material Lagarosiphon major (Institute
for Reference Materials and Measurements, IRMM, BCR® no 060).
Student's t-test (α = 0.05) was used to ascertain whether analyzed
values for the reference material were in significant agreement with
the certified values. The percent recovery reported values between 90
and 105%. Detection limits were expressed as three times the standard
deviation from the mean blank, and analyses were carried out in
triplicates.
2.4. Statistical processing
A one-way ANOVA was performed to detect possible differences be-
tween the levels of trace elements in the various different plant organs.
Prior to performing ANOVA, the Shapiro-Wilk test was carried out to de-
termine the normal distribution of the data sets, and the Levene's test to
check the hypothesis of homoscedasticity. In case of not normal distri-
bution, data were log-transformed. Tukey's post hoc test was then per-
formed to identify which specific mean pairs differ significantly.
Possible correlation between water/sediments and plant species were
assessed with Student's t-test. The level of significance was set at 0.05,
and statistical processing was carried out with the statistical software
IBM SPSS Version 22.0.
Bioconcentration and translocation factors were calculated to as-
sess element mobility from sediments to plants, and across plant
organs:
• Bioconcentration Factor (BCF): Croot/Csediment
where Csediment and Croot are the concentrations of a given trace element
respectively in sediment and roots of a species (mg kg−1 DW); BCF is a
measure of the efficiency of a plant species to take up a specific element
from sediments, and accumulate it in its tissues (EPA, 2007);
• Translocation factors (TF): Cleaf/Croot, Cstem/Croot, Cleaf/Cstem
where Cleaf, Croot and Cstem are the concentrations of a given trace ele-
ment respectively in leaves, roots and stems of a species (mg kg−1
DW); TF is a measure of the internal mobility of a given element across
plant organs (Deng et al., 2004).

Table 5
Values of the leaf/root translocation factor per element in the studied species.

Name As Cd Cr Cu Hg Mn Ni Pb Zn Mean

Alisma plantago-aquatica 0.44 0.57 0.78 0.81 0.10 0.46 0.58 0.30 0.45 0.48
Apium nodiflorum 0.48 0.90 0.59 0.77 0.50 0.79 0.53 0.44 0.65 0.61
Arundo donax 0.33 0.30 0.61 0.48 0.31 0.52 0.28 0.16 0.43 0.38
Bolboschoenus maritimus 0.41 0.77 0.53 0.68 0.81 0.58 0.61 0.44 0.66 0.61
Carex cuprina 0.68 0.77 0.71 0.75 0.70 0.75 0.77 0.73 0.59 0.72
Cyperus longus 0.12 0.69 0.62 0.59 0.71 0.78 0.74 0.70 0.58 0.61
Eichhornia crassipes 0.53 0.79 0.83 0.81 0.79 0.74 0.70 0.62 0.78 0.73
Epilobium hirsutum 0.61 0.68 0.66 0.73 0.70 0.74 0.63 0.61 0.82 0.68
Equisetum arvense 0.57 0.54 0.47 0.60 0.53 0.56 0.39 0.36 0.58 0.52
Juncus acutus 0.45 0.63 0.56 0.52 0.75 0.62 0.41 0.63 0.61 0.58
Juncus maritimus 0.67 0.64 0.68 0.54 1.37 1.49 1.38 1.40 1.33 1.06
Lemna minor 1.13 1.21 1.17 1.10 1.08 1.22 1.31 1.20 1.11 1.18
Lemna gibba 1.32 1.20 1.29 1.19 1.09 1.19 1.26 1.10 0.84 1.15
Nasturtium officinale 0.38 0.56 0.63 0.78 0.67 0.51 0.53 0.67 0.64 0.60
Paspalum paspaloides 0.48 0.88 0.57 0.55 0.60 0.62 0.35 0.42 0.53 0.56
Phragmites australis 0.15 0.75 0.65 0.57 0.79 0.84 0.67 0.24 0.49 0.57
Typha angustifolia 0.16 0.37 0.35 0.28 0.38 0.18 0.33 0.14 0.64 0.33
Typha domingensis 0.14 0.28 0.31 0.41 0.58 0.19 0.22 0.13 0.66 0.35
Typha latifolia 0.17 0.20 0.30 0.49 0.53 0.16 0.38 0.16 0.43 0.31
Veronica anagallis-aquatica 0.57 0.62 0.68 0.88 0.51 0.45 0.53 0.48 0.53 0.58
Mean 0.49 0.67 0.64 0.68 0.66 0.70 0.63 0.54 0.67
256 G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261

Table 6
Values of the stem/root translocation factor per element in the studied species.

Name As Cd Cr Cu Hg Mn Ni Pb Zn Mean

Alisma plantago-aquatica 0.23 0.29 0.40 0.59 0.30 0.19 0.34 0.16 0.25 0.31
Apium nodiflorum 0.32 0.51 0.32 0.64 0.26 0.37 0.28 0.31 0.46 0.39
Arundo donax 0.17 0.22 0.19 0.16 0.16 0.21 0.14 0.03 0.27 0.17
Bolboschoenus maritimus 0.11 0.32 0.26 0.33 0.18 0.14 0.12 0.20 0.17 0.19
Carex cuprina 0.22 0.61 0.41 0.49 0.45 0.43 0.41 0.45 0.20 0.41
Cyperus longus 0.07 0.21 0.14 0.22 0.24 0.10 0.11 0.08 0.23 0.16
Eichhornia crassipes 0.09 0.41 0.38 0.54 0.41 0.12 0.39 0.19 0.37 0.32
Epilobium hirsutum 0.49 0.54 0.34 0.53 0.38 0.40 0.34 0.42 0.51 0.44
Equisetum arvense 0.66 0.71 0.56 0.70 0.66 0.73 0.48 0.52 0.65 0.63
Juncus acutus 0.57 0.77 0.68 0.72 0.92 0.74 0.65 0.85 0.89 0.74
Juncus maritimus 0.83 0.70 0.81 0.75 0.79 0.63 0.86 0.65 0.71 0.75
Nasturtium officinale 0.19 0.29 0.32 0.59 0.35 0.26 0.34 0.39 0.33 0.35
Paspalum paspaloides 0.24 0.69 0.29 0.32 0.21 0.19 0.13 0.24 0.27 0.29
Phragmites australis 0.08 0.34 0.19 0.23 0.25 0.13 0.14 0.08 0.16 0.18
Typha angustifolia 0.24 0.57 0.49 0.75 0.71 0.34 0.74 0.26 0.87 0.56
Typha domingensis 0.27 0.43 0.47 0.73 0.78 0.41 0.63 0.18 0.82 0.52
Typha latifolia 0.25 0.30 0.42 0.85 0.80 0.52 0.78 0.30 0.69 0.50
Veronica anagallis-aquatica 0.41 0.27 0.39 0.46 0.28 0.22 0.34 0.17 0.25 0.32
Mean 0.28 0.41 0.36 0.48 0.40 0.31 0.36 0.27 0.43

3. Results translocation factors in plants were in the range of 0.16–0.75

The levels of trace elements in waters and sediments showed no sig-
nificant differences in the four study periods, implying a relatively con-
stant input from polluting sources (Tables 2 and 3). According to the
available Italian limits of concentrations, the levels of As, Cr, Hg, Ni
and Pb in waters were generally close to or higher than the legal limits.
In particular, the levels of Hg in waters reached concentrations up to five
times higher than the legal limits. Regarding the levels of trace elements
in sediments, the concentrations of As were around the legal limits
whereas the concentrations of Cd, Hg, Ni and Pb passed the permissible
levels. The mean values of the bioconcentration factor ranged between
0.04 and 0.65 (Table 4). In particular, E. crassipes and P. australis showed
the highest bioconcentration factors (0.65 and 0.53, respectively),
whereas N. officinale and A. nodiflorum exhibited the lowest values
(0.03 and 0.04). Mercury showed the highest translocation from sedi-
ments to roots, whereas Cr, Ni and Pb showed the lowest root/sediment
mobility. Regarding the leaf/root element translocation (Table 5), the
highest mean values were found in L. minor and L. gibba (1.18 and
1.15, respectively), whereas the lowest values were found in
T. domingensis, T. angustifolia and T. latifolia (0.35, 0.33 and 0.31). The
leaf/root translocation exhibited a narrow range of values in the case
of the elements (0.49–0.70), of which Mn and As reported the highest
and lowest scores (0.70 and 0.49, respectively). The stem/root
(Table 6), and specifically, J. maritimus and J. acutus exhibited the
highest values (0.75 and 0.74, respectively), whereas the lowest values
were found in P. australis (0.18), A. donax (0.17) and C. longus (0.16). Re-
garding elements, Cu, Cd and Hg showed the highest stem/root translo-
cation (0.48, 0.41 and 0.40), whereas the lowest translocation was
found in As and Pb (0.28 and 0.27). The highest values of the leaf/
stem translocation were found in C. longus (3.71), B. maritimus (3.25),
P. australis (3.23), and E. crassipes (3.18), whereas T. domingensis
(0.62), T. latifolia (0.60) and T. angustifolia (0.58) showed the lowest
values (Table 7). The element Mn showed by far the highest leaf/stem
translocation (2.41), whereas Cd and Cu reported the lowest values
(1.54 and 1.45).
Table 8 shows that trace element compartmentalization is a consis-
tent pattern in all studied species whose levels of concentrations were
generally different between the various kinds of organ. Specifically,
the levels of concentrations generally decreased in the order of roots
N leaves N stems, with the exception of the three Typha species whose
trend was roots N stems N leaves. The correlation between trace element
concentrations in plants and water/sediments was significantly variable
in the studied species. In particular, a positive correlation between plant
and water/sediments was found in B. maritimus, C. cuprina, C. longus,
L. minor, L. gibba, and P. australis. Instead, the other plants showed a sig-
nificant correlation mainly with sediments and only for some elements.

Table 7
Values of the leaf/stem translocation factor per element in the studied species.

Name As Cd Cr Cu Hg Mn Ni Pb Zn Mean

Alisma plantago-aquatica 1.92 2.03 1.90 1.39 1.68 2.39 1.73 1.83 1.86 1.83
Apium nodiflorum 1.52 1.83 1.86 1.26 2.10 2.15 1.91 1.42 1.44 1.72
Arundo donax 2.06 1.53 3.21 3.07 2.12 2.49 1.97 5.12 1.61 2.53
Bolboschoenus maritimus 3.70 2.47 2.09 2.03 4.62 4.11 4.57 2.24 3.91 3.25
Carex cuprina 3.15 1.27 1.73 1.53 1.62 1.75 1.72 1.68 3.12 1.96
Cyperus longus 1.82 3.21 4.49 2.70 3.37 5.07 6.10 3.46 3.06 3.71
Eichhornia crassipes 8.03 1.98 2.21 1.51 1.94 6.12 1.83 3.08 2.16 3.18
Epilobium hirsutum 1.25 1.28 1.78 1.43 1.76 2.03 1.81 1.48 1.58 1.60
Equisetum arvense 0.88 0.75 0.83 0.87 0.81 0.74 0.79 0.77 0.89 0.81
Juncus acutus 0.79 0.83 0.81 0.77 0.84 0.82 0.65 0.69 0.67 0.75
Juncus maritimus 0.82 0.86 0.84 0.72 0.48 0.91 0.76 0.86 0.82 0.78
Nasturtium officinale 2.04 2.10 2.40 1.33 2.12 1.94 1.52 1.81 1.94 1.90
Paspalum paspaloides 2.11 1.27 2.06 1.72 3.05 3.15 2.67 1.72 1.98 2.19
Phragmites australis 1.92 2.21 3.34 2.44 3.17 6.21 4.45 3.12 3.03 3.23
Typha angustifolia 0.69 0.64 0.73 0.39 0.52 0.54 0.45 0.56 0.71 0.58
Typha domingensis 0.59 0.65 0.70 0.56 0.75 0.46 0.34 0.72 0.75 0.62
Typha latifolia 0.61 0.67 0.71 0.52 0.71 0.48 0.31 0.76 0.77 0.60
Veronica anagallis-aquatica 1.41 2.28 1.68 1.91 1.78 2.05 1.58 2.89 2.19 1.96
Mean 1.95 1.54 1.85 1.45 1.87 2.41 1.95 1.90 1.81
 G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261
For this group of plants, roots were the main organs to be correlated
with trace elements in sediments. Overall, the studied plants showed
significantly higher levels of trace elements compared to the control
area.
4. Discussion
The studied plants showed a general capacity to tolerate significant
levels of trace element contamination, both in water and sediments. In
particular, the results showed that these plants could tolerate higher
concentrations of As, Cr, Hg, Ni and Pb in waters according to the Italian
legal limits. Plant species were also tolerant to high levels of Cd, Hg, Ni
and Pb in sediments. The essential elements of this study included Cu,
Mn and Zn (micronutrients). These elements showed, in all cases,
higher concentrations than non-essential or toxic elements. This is gen-
erally due to the greater capacity of plants to uptake micronutrients
compared to non-essential elements for which plants may develop tol-
erance strategies that reduce their uptake and accumulation (Kabata-
Pendias, 2011). However, even essential elements like Cu, Mn and Zn
may prove toxic if accumulated at high concentrations, but this was
not the case of our study. In general, plant tolerance to high element
concentrations is a function of numerous factors such as phenology,
vigor, growth, element speciation, and water chemistry (Yang and Ye,
2009). However, element compartmentalization itself should be consid-
ered as a tolerance strategy because it allows plant species to reduce the
translocation of trace elements from underground to photosynthetic
aboveground organs. Element compartmentalization was a common
pattern in all studied plants whose various organs showed significantly
different levels of trace elements. In line with previous findings (e.g.
Salem et al., 2014; Liu et al., 2016; Bonanno and Cirelli, 2017), this
study found that the levels of element concentrations generally de-
creased in the order of roots N leaves N stems, with the exception of
the three Typha species whose trend was root N stem N leaf, which is
typical of the Typha genus (Carranza-Álvarez et al., 2008). The compart-
mentalization strategy is consistent in numerous wetland plants, and
essentially consists of accumulating the highest levels of trace element
concentrations in the underground organs, as a defensive mechanism
to protect the species against the harmful effects of toxic levels on pho-
tosynthetic processes (e.g., Willis et al., 2010; Bonanno, 2013; Phillips
et al., 2015). The greater accumulation of trace elements in under-
ground organs was a common pattern in all studied plants, in line
with most authors (e.g. Bonanno, 2011, 2012; Eid et al., 2012; Engin
et al., 2017). The fact that the bulk of these elements is accumulated in
roots may suggest a significant presence of mobile chemical species in
sediments but it may also imply the existence of tolerance strategies
that prevent toxic concentrations in roots from translocating to the
aboveground organs (Hozhina et al., 2001; Bonanno et al., 2017). Wet-
land plants can indeed accumulate high levels of trace elements in be-
lowground organs as a consequence of multiple factors such as
internal detoxification capacity of underground organs, accumulation
capacity of root cell walls and intercellular air spaces characterizing
the cortex parenchyma (Hall, 2002; Mishra et al., 2008). The role of be-
lowground organs as the accumulators of the bulk element concentra-
tions supports the scientific evidence according to which wetland
plants are suitable for applications of ecological restoration such as
phytostabilization (Willis et al., 2010; Lyubenova et al., 2013; Gomes
et al., 2014).
This study showed that element translocation from sediments to
roots was highly variable among the various elements and among the
various plant species. In turn, element translocation across internal tis-
sues was significantly variable among species but was in a narrower
range among various elements. These findings may suggest that ele-
ment translocation from sediment to roots is mainly species- and
element-specific, whereas translocation across internal tissues is more
species-specific. Plant species can take up and accumulate higher
amounts of trace elements as a consequence of numerous factors
257
among which selective uptake of ions, decreased permeability of cell
walls or other differences in the structure and function of membranes,
immobilization of ions in various organs (synthesis of immobilizing
compounds including the formation of minerals, and/or fixation by
charged ligands), alteration in metabolic patterns (increased enzyme
system that is inhibited, or increased antagonistic metabolite, or re-
duced metabolic pathway by passing an inhibited site, or decreased re-
quirement for products of inhibited synthesis), and adaptation to toxic
metal replacement of a physiological metal in an enzyme (Kabata-
Pendias and Mukherjee, 2007). In general, plant species are less suitable
for phytoextraction of trace elements when the factor of element trans-
location from roots to aboveground organs is lower than unity (Ma
et al., 2001; Yoon et al., 2006; Pandey, 2012). This is in line with the re-
sults of this study that showed the majority of the wetland plants had a
leaf/root translocation factor b 1. In turn, both free-floating hydrophytes
L. minor and L. gibba showed a leaf/root translocation factor N 1 for all
trace elements, whereas the rhizomatous geophyte J. maritimus only
for Hg, Mn, Ni, Pb and Zn, thus resulting in a higher capacity of translo-
cation compared to the other wetland plants (Dirilgen, 2011; Sasmaz
et al., 2015). Regarding the element mobility from roots to stems, trans-
location factors were more variable among plants rather than among el-
ements, and showed their highest mean values in the congener species
J. maritimus and J. acutus, which, however have different life forms. The
highest values of the leaf/stem translocation were found in three rhizo-
matous helophytes C. longus, B. maritimus and P. australis, and in the
free-floating hydrophyte E. crassipes, whereas the three Typha species
(all rhizomatous helophytes) showed the lowest element mobility
from stems to leaves. The leaf/stem translocation was overall high for
all elements, in particular, Mn showed the highest mobility, which is
likely due to its important metabolic role (Memon et al., 2001). In gen-
eral, element translocation from sediment to roots and within plant tis-
sues is dependent on many factors such as pH, reduction potential,
temperature, salinity, organic matter content and levels of other ele-
ments (Greger, 1999; Yang and Ye, 2009). However, other factors in-
cluding seasonal variation in physiology and compartmentalization
capacity may also influence the level of accumulation in plant species
(Laffont-Schwob et al., 2015; Vymazal, 2016; Bonanno et al., 2017).
The studied plants showed significantly higher levels of trace ele-
ments compared to the control area, implying that plant species can re-
flect, although at a different degree, the level of pollution inputs (Wójcik
et al., 2014). In particular, this study found that some congener plants
show similar magnitude of element accumulation and translocation
(e.g. Typha ssp.), whereas others do not (e.g. Juncus ssp.). Another find-
ing showed that similar life forms do not imply similar concentrations.
For example, the two species A. plantago-aquatica and A. nodiflorum,
both rooted hydrophytes, showed significantly different levels of ele-
ment concentrations in their tissues; in turn, the free-floating hydro-
phyte E. crassipes and the rhizomatous helophyte P. australis showed
similar levels of trace elements. The element uptake of plants is gener-
ally influenced by several soil properties that include pH, cation ex-
change capacity, organic matter content or presence of various ionic
forms (Kabata-Pendias, 2011). However, as suggested by this study,
plant species may also respond differently to similar inputs of trace ele-
ments, according to their species-specific capacity to accumulate, trans-
locate and detoxify trace elements (Zabłudowska et al., 2009; Usman
et al., 2012). Other processes can determine conflicting or synergetic in-
teractions between trace elements that may affect uptake and translo-
cation in plant tissues (Prasad et al., 2006; Gall et al., 2015). In
particular, these processes may be associated with numerous factors
such as level of sediment contamination, plant seasonal physiology,
organ type, species-specific biochemical properties and compartmen-
talization capacity (Greger, 1999; Lyubenova et al., 2013).
The analysis of plant bioindication potential showed that the corre-
lation between all trace elements in plants and water/sediments was
significant only for B. maritimus, C. cuprina, C. longus, L. minor, L. gibba,
and P. australis. Previous findings supported these results but case
 258
G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261
Table 8
Levels of trace elements in the studied species and correlation with water and sediments [mean values ± SD mg kg−1].

Name Organs As Cd Cr Cu Hg Mn Ni Pb Zn

Alisma plantago-aquatica
Apium nodiflorum
Arundo donax
Bolboschoenus maritimus
Carex cuprina
Cyperus longus
Eichhornia crassipes
Epilobium hirsutum
Equisetum arvense
Juncus acutus
Root 0.52 ± 0.06a,⁎,K 0.14 ± 0.02a,°,⁎,K 0.32 ± 0.08a,°,⁎,K 4.04 ± 0.41a,°,⁎,K 0.10 ± 0.02a,K 38.8 ± 5.41a,°,⁎,K 1.24 ± 0.31a,°,⁎,K 1.86 ± 0.09a,K 27.8 ± 4.23a,°,⁎,K
Stem 0.12 ± 0.02b 0.04 ± 0.007b 0.13 ± 0.02b 2.38 ± 0.30b,°,⁎ 0.03 ± 0.005b 7.46 ± 1.12b,°,⁎ 0.42 ± 0.06b 0.30 ± 0.03b 6.80 ± 0.90b,°,⁎
Leaf 0.23 ± 0.03c 0.08 ± 0.01c,K 0.25 ± 0.03c 3.28 ± 0.42c,°,⁎ 0.05 ± 0.01c,K 17.8 ± 3.45c,°,⁎ 0.72 ± 0.08c,K 0.55 ± 0.07c 12.5 ± 2.25c,°,⁎
Root 0.31 ± 0.04a,K 0.10 ± 0.02a,K 0.22 ± 0.03a,K 2.32 ± 0.25a,⁎,K 0.04 ± 0.01a,K 7.56 ± 1.21a,⁎,K 0.79 ± 0.09a,K 0.32 ± 0.05a,⁎,K 6.78 ± 0.89a,⁎,K
Stem 0.10 ± 0.01b 0.05 ± 0.01b 0.07 ± 0.01b 1.49 ± 0.21b 0.01 ± 0.002b 2.78 ± 0.34b 0.22 ± 0.05b 0.10 ± 0.02b 3.12 ± 0.04b
Leaf 0.15 ± 0.02c 0.09 ± 0.01c 0.13 ± 0.02c,K 1.88 ± 0.23c 0.02 ± 0.003c 5.97 ± 0.71c 0.42 ± 0.04c 0.14 ± 0.03c 4.45 ± 0.56c
Root 0.29 ± 0.04a,K 0.10 ± 0.02a,K 1.17 ± 0.21a,K 5.55 ± 0.67a,⁎,K 0.25 ± 0.03a,K 16.7 ± 2.34a,⁎,K 3.15 ± 0.42a,K 1.34 ± 0.18a,K 6.29 ± 0.85a,⁎,K
Stem 0.05 ± 0.01b 0.02 ± 0.003b,K 0.22 ± 0.03b 0.88 ± 0.10b 0.04 ± 0.01b,K 3.44 ± 0.42b,K 0.45 ± 0.65b 0.04 ± 0.01b,K 1.68 ± 0.23b
Leaf 0.10 ± 0.02c,K 0.03 ± 0.005c,K 0.71 ± 0.09c,K 2.69 ± 0.32c,K 0.08 ± 0.02c,K 8.56 ± 1.23c,K 0.88 ± 0.10c,K 0.21 ± 0.03c,K 2.69 ± 0.35c,K
Root 1.85 ± 0.23a,°,⁎,K 1.05 ± 0.20a,°,⁎,K 3.25 ± 0.26a,°,⁎,K 19.5 ± 2.65a,°,⁎,K 0.62 ± 0.08a,°,⁎,K 258 ± 35.8a,°,⁎,K 3.12 ± 0.45a,°,⁎,K 7.12 ± 1.02a,°,⁎,K 110 ± 12.5a,°,⁎,K
Stem 0.20 ± 0.03b,°,⁎,K 0.33 ± 0.03b,°,⁎,K 0.82 ± 0.11b,°,⁎,K 6.35 ± 0.96b,°,⁎,K 0.11 ± 0.02b,°,⁎,K 36.9 ± 5.25b,°,⁎,K 0.41 ± 0.07b,°,⁎,K 1.38 ± 0.26b,°,⁎,K 18.5 ± 2.90b,°,⁎,K
Leaf 0.75 ± 0.10c,°,⁎,K 0.81 ± 0.10c,°,⁎,K 1.71 ± 0.28c,°,⁎,K 13.2 ± 2.04c,°,⁎,K 0.51 ± 0.07c,°,⁎,K 153 ± 21.8c,°,⁎,K 1.89 ± 0.25c,°,⁎,K 3.09 ± 0.51c,°,⁎,K 72.9 ± 9.92c,°,⁎,K
Root 1.53 ± 0.22a,°,⁎,K 1.25 ± 0.13a,°,⁎,K 2.35 ± 0.31a,°,⁎,K 16.4 ± 2.02a,°,⁎,K 0.45 ± 0.05a,°,⁎,K 89.4 ± 35.2a,°,⁎,K 2.01 ± 0.35a,°,⁎,K 4.34 ± 0.54a,°,⁎,K 89.5 ± 10.2a,°,⁎,K
Stem 0.33 ± 0.05b,°,⁎,K 0.75 ± 0.09b,°,⁎,K 0.96 ± 0.11b,°,⁎,K 7.96 ± 1.45b,°,⁎,K 0.20 ± 0.03b,°,⁎,K 38.7 ± 5.67b,°,⁎,K 0.87 ± 0.10b,°,⁎,K 1.89 ± 0.26b,°,⁎,K 17.4 ± 2.32b,°,⁎,K
Leaf 1.04 ± 0.12c,°,⁎,K 0.96 ± 0.10c,°,⁎,K 1.68 ± 0.22c,°,⁎,K 12.3 ± 2.01c,°,⁎,K 0.32 ± 0.05c,°,⁎,K 67.5 ± 13.2c,°,⁎,K 1.54 ± 0.35c,°,⁎,K 3.25 ± 0.41c,°,⁎,K 52.5 ± 7.23c,°,⁎,K
Root 2.65 ± 0.19a,°,⁎,K 1.05 ± 0.15a,°,⁎,K 3.25 ± 0.31a,°,⁎,K 22.3 ± 3.56a,°,⁎,K 0.65 ± 0.06a,°,⁎,K 387 ± 45.7a,°,⁎,K 4.35 ± 0.45a,°,⁎,K 6.25 ± 1.20a,°,⁎,K 96.6 ± 10.7a,°,⁎,K
Stem 0.18 ± 0.02b,°,⁎,K 0.22 ± 0.03b,°,⁎,K 0.45 ± 0.03b,°,⁎,K 4.93 ± 0.55b,°,⁎,K 0.14 ± 0.02b,°,⁎,K 36.2 ± 4.97b,°,⁎,K 0.44 ± 0.05b,°,⁎,K 0.51 ± 0.06b,°,⁎,K 22.4 ± 4.52b,°,⁎,K
Leaf 0.33 ± 0.04c,°,⁎,K 0.73 ± 0.08c,°,⁎,K 2.01 ± 0.15c,°,⁎,K 13.3 ± 2.01c,°,⁎,K 0.47 ± 0.05c,°,⁎,K 187 ± 21.5c,°,⁎,K 2.74 ± 0.35c,°,⁎,K 1.85 ± 0.34c,°,⁎,K 67.5 ± 8.43c,°,⁎,K
Root 2.72 ± 0.30a,°,K 1.55 ± 0.32a,°,K 3.05 ± 0.31a,°,K 20.3 ± 3.02a,°,K 1.35 ± 0.21a,°,K 385 ± 45.7a,°,K 3.43 ± 0.50a,°,K 6.85 ± 1.45a,°,K 112 ± 16.5a,°,K
Stem 0.18 ± 0.03b,°,K 0.62 ± 0.08b,°,K 1.15 ± 0.19b,°,K 10.9 ± 2.12b,°,K 0.55 ± 0.07b,°,K 46.8 ± 6.69b,°,K 1.34 ± 0.21b,°,K 1.34 ± 0.23b,°,K 41.3 ± 6.89b,°,K
Leaf 1.45 ± 0.26c,°,K 1.23 ± 0.24c,°,K 2.54 ± 0.28c,°,K 16.5 ± 3.19c,°,K 1.07 ± 0.14c,°,K 286 ± 34.5c,°,K 2.44 ± 0.40c,°,K 4.11 ± 0.54c,°,K 88.5 ± 12.7c,°,K
Root 0.41 ± 0.04a,K 0.28 ± 0.02a,⁎,K 0.35 ± 0.03a,⁎,K 2.64 ± 0.25a,⁎,K 0.10 ± 0.01a,K 10.6 ± 1.51a,⁎,K 1.29 ± 0.29a,K 0.56 ± 0.07a,⁎,K 8.88 ± 1.92a,⁎,K
Stem 0.20 ± 0.01b 0.15 ± 0.01b 0.13 ± 0.02b 1.39 ± 0.21b,⁎,K 0.04 ± 0.002b 3.88 ± 0.44b,⁎ 0.45 ± 0.07b 0.23 ± 0.02b 4.56 ± 0.67b,⁎,K
Leaf 0.25 ± 0.02c,K 0.19 ± 0.01c,K 0.23 ± 0.02c,K 1.98 ± 0.23c,⁎,K 0.07 ± 0.003c 7.85 ± 0.98c,⁎,K 0.82 ± 0.09c,K 0.34 ± 0.03c 7.23 ± 0.72c,⁎,K
Root 0.61 ± 0.06a,⁎,K 0.35 ± 0.02a,⁎,K 0.45 ± 0.05a,⁎,K 8.45 ± 1.05a,⁎,K 0.15 ± 0.02a,⁎,K 57.9 ± 7.35a,⁎,K 2.81 ± 0.29a,⁎,K 2.42 ± 0.35a,⁎,K 66.8 ± 8.91a,⁎,K
Stem 0.40 ± 0.05b,K 0.25 ± 0.01b,K 0.25 ± 0.02b,K 5.89 ± 0.82b,⁎,K 0.10 ± 0.02b,⁎,K 42.8 ± 5.62b,K 1.42 ± 0.23b,K 1.26 ± 0.21b,K 43.2 ± 6.04b,⁎,K
Leaf 0.35 ± 0.02b,K 0.19 ± 0.01c,K 0.21 ± 0.02b,K 5.08 ± 056b,⁎,K 0.08 ± 0.01b,K 31.5 ± 4.71c,K 1.12 ± 0.19c,K 0.94 ± 0.10c,K 38.5 ± 5.96b,⁎,K
Root 1.86 ± 0.25a,⁎,K 0.95 ± 0.15a,⁎,K 2.58 ± 0.32a,⁎,K 15.7 ± 2.11a,⁎,K 0.65 ± 0.08a,⁎,K 104 ± 18.8a,⁎,K 4.72 ± 0.54a,⁎,K 4.03 ± 0.61a,⁎,K 74.1 ± 10.2a,⁎,K

Juncus maritimus
Lemna minor
Lemna gibba
Nasturtium officinale
Paspalum paspaloides
Phragmites australis
Stem 1.06 ± 0.15b,K 0.75 ± 0.09b,K 1.78 ± 0.24b,K 10.9 ± 2.25b,⁎,K 0.60 ± 0.05a,K 78.5 ± 14.3b,⁎,K 3.06 ± 0.46b,K 3.68 ± 0.42b,K 67.3 ± 7.03b,⁎,K
Leaf 0.84 ± 0.10c,K 0.60 ± 0.08c,K 1.45 ± 0.19c,K 8.65 ± 1.25c,⁎,K 0.49 ± 0.06b,K 64.9 ± 11.5c,⁎,K 1.96 ± 0.34c,K 2.51 ± 0.32c,K 45.5 ± 5.67c,⁎,K
Root 1.98 ± 0.22a,⁎,K 1.35 ± 0.17a,⁎,K 2.80 ± 0.41a,⁎,K 21.9 ± 4.05a,⁎,K 0.85 ± 0.10a,⁎,K 154 ± 23.5a,⁎,K 3.42 ± 0.40a,⁎,K 5.83 ± 0.86a,⁎,K 83.8 ± 13.5a,⁎,K
Stem 1.66 ± 0.19b,K 1.02 ± 0.12b,K 2.28 ± 0.31b,K 16.5 ± 3.45b,⁎,K 0.67 ± 0.08a,K 96.5 ± 15.1b,⁎,K 2.93 ± 0.32b,K 3.75 ± 0.45b,K 60.5 ± 10.1b,⁎,K
Leaf 1.34 ± 0.12c,K 0.87 ± 0.10c,K 1.90 ± 0.23c,K 11.8 ± 2.35c,⁎,K 0.32 ± 0.05b,K 87.9 ± 11.5c,⁎,K 2.22 ± 0.19c,K 3.21 ± 0.32c,K 50.8 ± 7.45c,⁎,K
Root 1.86 ± 0.22a,°,⁎,K 0.42 ± 0.06a,°,⁎,K 3.33 ± 0.38a,°,⁎,K 14.0 ± 2.12a,°,⁎,K 0.68 ± 0.08a,°,⁎,K 221 ± 18.8a,°,⁎,K 3.02 ± 0.42a,°,⁎,K 6.12 ± 0.76a,°,⁎,K 81.5 ± 10.2a,°,⁎,K
Leaf 2.10 ± 0.35a,°,⁎,K 0.51 ± 0.06b,°,⁎,K 3.86 ± 0.47a,°,⁎,K 16.3 ± 2.23a,°,⁎,K 0.74 ± 0.09a,°,⁎,K 265 ± 31.4b,°,⁎,K 3.89 ± 0.45b,°,⁎,K 7.45 ± 0.95a,°,⁎,K 92.7 ± 12.2a,°,⁎,K
Root 1.46 ± 0.15a,°,⁎,K 0.35 ± 0.05a,°,⁎,K 2.45 ± 0.29a,°,⁎,K 11.0 ± 1.88a,°,⁎,K 0.55 ± 0.06a,°,⁎,K 189 ± 21.7a,°,⁎,K 1.75 ± 0.21a,°,⁎,K 5.02 ± 0.56a,°,⁎,K 64.8 ± 8.34a,°,⁎,K
Leaf 1.93 ± 0.18a,°,⁎,K 0.42 ± 0.05a,°,⁎,K 3.16 ± 0.41a,°,⁎,K 11.9 ± 2.01a,°,⁎,K 0.60 ± 0.06a,°,⁎,K 225 ± 26.5b,°,⁎,K 2.21 ± 0.33b,°,⁎,K 5.51 ± 0.65a,°,⁎,K 77.5 ± 10.1b,°,⁎,K
Root 0.26 ± 0.03a,K 0.07 ± 0.01a,K 0.16 ± 0.04a,K 2.02 ± 0.20a,⁎,K 0.03 ± 0.01a,K 6.45 ± 0.74a,⁎,K 0.62 ± 0.05a,K 0.43 ± 0.05a,K 7.85 ± 1.19a,⁎,K
Stem 0.05 ± 0.01b 0.02 ± 0.003b 0.05 ± 0.01b 1.19 ± 0.15b 0.01 ± 0.002b 1.65 ± 0.22b 0.21 ± 0.02b 0.16 ± 0.02b 2.58 ± 0.03b
Leaf 0.10 ± 0.02c 0.04 ± 0.01c 0.12 ± 0.02c,K 1.58 ± 0.17c,⁎,K 0.02 ± 0.002c 3.22 ± 0.45c,K 0.32 ± 0.03c 0.29 ± 0.03c 5.02 ± 0.67c,K
Root 0.21 ± 0.03a,K 0.16 ± 0.02a,K 0.28 ± 0.03a,K 3.78 ± 0.45a,⁎,K 0.05 ± 0.01a,K 10.5 ± 1.99a,⁎,K 0.92 ± 0.09a,K 0.41 ± 0.05a,⁎,K 7.89 ± 1.12a,⁎,K
Stem 0.05 ± 0.01b 0.11 ± 0.01b 0.08 ± 0.01b,K 1.21 ± 0.18b,K 0.01 ± 0.002b 2.08 ± 0.37b 0.12 ± 0.01b 0.10 ± 0.02b 2.10 ± 0.03b,K
Leaf 0.10 ± 0.02c,K 0.14 ± 0.01a 0.16 ± 0.02c,K 2.08 ± 0.20c,K 0.03 ± 0.004c,K 6.38 ± 0.73c,K 0.32 ± 0.03c 0.17 ± 0.02c,K 4.15 ± 0.61c,K
Root 2.85 ± 0.34a,°,⁎,K 1.25 ± 0.21a,°,⁎,K 3.45 ± 0.41a,°,⁎,K 25.6 ± 3.44a,°,⁎,K 0.85 ± 0.09a,°,⁎,K 438 ± 55.2a,°,⁎,K 4.55 ± 0.55a,°,⁎,K 8.45 ± 1.12a,°,⁎,K 135 ± 15.7a,°,⁎,K
Stem 0.23 ± 0.04b,°,⁎,K 0.42 ± 0.06b,°,⁎,K 0.65 ± 0.08b,°,⁎,K 5.86 ± 0.65b,°,⁎,K 0.21 ± 0.04b,°,⁎,K 56.7 ± 7.67b,°,⁎,K 0.64 ± 0.09b,°,⁎,K 0.66 ± 0.07b,°,⁎,K 21.4 ± 3.32b,°,⁎,K
Leaf 0.44 ± 0.06c,°,⁎,K 0.93 ± 0.09c,°,⁎,K 2.21 ± 0.25c,°,⁎,K 14.3 ± 2.21c,°,⁎,K 0.67 ± 0.09c,°,⁎,K 367 ± 41.5c,°,⁎,K 3.04 ± 0.45c,°,⁎,K 2.05 ± 0.24c,°,⁎,K 66.5 ± 8.43c,°,⁎,K

G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261

Typha angustifolia Root 1.76 ± 0.23a,⁎,K 1.00 ± 0.12a,⁎,K 2.15 ± 0.25a,⁎,K 15.4 ± 1.82a,°,⁎,K 0.58 ± 0.07a,⁎,K 194 ± 24.8a,°,⁎,K 4.37 ± 0.52a,⁎,K 6.88 ± 0.79a,⁎,K 94.3 ± 12.6a,°,⁎,K
Stem 0.42 ± 0.06b,K 0.55 ± 0.06b,K 1.03 ± 0.10b,K 11.5 ± 1.35b,⁎,K 0.42 ± 0.06b,K 66.2 ± 8.45b,⁎,K 3.26 ± 0.36b,K 1.78 ± 0.20b,K 83.8 ± 11.5a,⁎,K
Leaf 0.29 ± 0.04c,K 0.35 ± 0.05c,K 0.75 ± 0.08c,K 4.35 ± 0.55c,⁎,K 0.22 ± 0.03b,K 35.5 ± 5.66c,⁎,K 1.45 ± 0.18c,K 0.95 ± 0.11b,K 57.9 ± 7.12c,⁎,K
Typha domingensis Root 2.06 ± 0.31a,⁎,K 1.05 ± 0.15a,⁎,K 3.03 ± 0.45a,°,⁎,K 18.7 ± 2.22a,°,⁎,K 0.72 ± 0.09a,⁎,K 234 ± 31.8a,°,⁎,K 5.67 ± 0.75a,⁎,K 5.78 ± 0.67a,⁎,K 104 ± 15.6a,°,⁎,K
Stem 0.56 ± 0.07b,K 0.45 ± 0.07b,K 1.38 ± 0.17b,K 13.6 ± 1.85b,⁎,K 0.56 ± 0.08b,K 96.5 ± 10.3b,⁎,K 3.56 ± 0.56b,K 1.02 ± 0.16b,K 87.9 ± 10.2b,⁎,K
Leaf 0.33 ± 0.05c,K 0.30 ± 0.04c,K 0.95 ± 0.10c,K 7.65 ± 0.95c,⁎,K 0.42 ± 0.07b,K 44.3 ± 6.45c,⁎,K 1.23 ± 0.21c,K 0.75 ± 0.10b,K 65.5 ± 8.48c,⁎,K
Typha latifolia Root 2.66 ± 0.35a,⁎,K 1.12 ± 0.10a,⁎,K 2.58 ± 0.34a,°,⁎,K 13.8 ± 1.67a,°,⁎,K 0.86 ± 0.09a,⁎,K 204 ± 26.5a,°,⁎,K 5.12 ± 0.64a,⁎,K 4.95 ± 0.54a,⁎,K 111 ± 19.8a,°,⁎,K
Stem 0.72 ± 0.09b,K 0.33 ± 0.05b,K 1.09 ± 0.11b,K 11.7 ± 1.21b,⁎,K 0.68 ± 0.07b,K 105 ± 12.5b,⁎,K 4.03 ± 0.51a,K 1.45 ± 0.21b,K 75.5 ± 8.91b,⁎,K
Leaf 0.44 ± 0.06c,K 0.22 ± 0.03c,K 0.77 ± 0.08c,K 6.88 ± 1.02c,⁎,K 0.51 ± 0.07c,K 39.7 ± 5.75c,⁎,K 1.95 ± 0.31b,K 0.97 ± 0.11c,K 45.5 ± 6.02c,⁎,K
Veronica anagallis-aquatica Root 0.67 ± 0.08a,⁎,K 0.26 ± 0.03a,°,⁎,K 0.47 ± 0.06a,°,⁎,K 4.53 ± 0.51a,°,⁎,K 0.18 ± 0.03a,K 47.7 ± 6.49a,°,⁎,K 2.48 ± 0.42a,°,⁎,K 3.55 ± 0.44a,K 44.5 ± 6.78a,°,⁎,K
Stem 0.27 ± 0.03b,K 0.07 ± 0.01b,K 0.19 ± 0.03b,K 2.08 ± 0.31b,°,⁎,K 0.05 ± 0.01b,K 10.7 ± 2.01b,°,⁎,K 0.84 ± 0.10b,K 0.60 ± 0.07b,K 10.8 ± 2.85b,°,⁎,K
Leaf 0.38 ± 0.05c,K 0.16 ± 0.02c,K 0.32 ± 0.04c,K 3.99 ± 0.21c,°,⁎,K 0.09 ± 0.02c,K 21.5 ± 3.88c,°,⁎,K 1.32 ± 0.16c,K 1.72 ± 0.30c,K 23.5 ± 4.10c,°,⁎,K

Note: different letters express significant differences between the diverse organs of the same species for one specific element (one-way ANOVA, p b 0.05); “°” expresses correlation between organ and water (t-test, p b 0.05); “⁎” expresses correlation
between organ and sediments (t-test, p b 0.05); “K” expresses significant differences in trace element concentrations between plants in control and study areas (t-test, p b 0.05); N = 400 observations in total per each study month and year.

259
260 G. Bonanno et al. / Science of the Total Environment 631–632 (2018) 252–261
studies on the element bioindication capacity of C. cuprina and C. longus
are relatively scarce (Zurayk et al., 2001; Favas et al., 2012; Guittonny-
Philippe et al., 2015a; Phillips et al., 2015). The other plants showed a
positive correlation mainly with sediments and only for some elements.
For such species, in particular, roots acted as the principal organs to be
correlated with trace elements in sediments. Roots are indeed the
main pathways of trace element uptake to plants, and as a result, rooted
species tend to reflect the levels of trace elements in sediments (Bothe
and Słomka, 2017). Positive correlations between sediments and roots
suggest the important role of sediments as the main source of elements
for wetland plants. This is generally confirmed in previous studies
showing that elements taken by rooted macrophytes are mainly sedi-
ment derived (Aksoy et al., 2005; Kabata-Pendias, A., 2011). Overall,
these wetland plants reflected the level of pollution in the study area
but only the element concentrations in some of them were also signifi-
cantly correlated with the environment, especially sediments. As a re-
sult, although wetland plants tend to concentrate the bulk of trace
element concentrations in the underground organs (regardless of the
root system, be the species rhizomatous or free-floating), these plants
may show also significant levels of element translocation to stems and
leaves in case of high concentrations in water and sediments. Previous
studies showed that element accumulation in aboveground organs are
mainly dependent on element bioavailability in sediments, species-
specific uptake, translocation capacity and the role of a given elements
in biological functions such enzymatic and metabolic processes
(Kabata-Pendias and Mukherjee, 2007; Teuchies et al., 2013). This
study corroborated previous findings on the potential use of wetland
plants as bioindicators of trace elements in water and, especially, in sed-
iments (Bonanno and Lo Giudice, 2010; Böcük et al., 2013; Guittonny-
Philippe et al., 2015b). However, this study showed also that the poten-
tial for bioindication is significantly different between species, and no
clear patterns of bioindication capacity were identified according to
the various plant life forms.
As pointed out by this study, different ecology (e.g. aquatic vs terres-
trial) and morphology (e.g. rhizomatous vs free-floating) do not neces-
sary imply different capacity of accumulation or bioindication of trace
elements. In particular, this study corroborated previous findings ac-
cording to which trace element translocation, from water and sedi-
ments, and across plant tissues, depends on kind of element and
species rather than being associated with a particular group of plant
life forms (Phillips et al., 2015; Engin et al., 2017). However, the fact
that translocation factors per element are generally in a narrower
range whereas translocation factors per species are more variable,
may suggest that the different element translocation is more species-
specific rather than element-specific. In turn, wetland plants share
also some important patterns that include element compartmentaliza-
tion in different organs, and bulk element concentrations in roots.
Trace elements may have toxic effects on the environment, thus affect-
ing irreparably the precarious stability of sensitive ecosystems such as
wetlands (Gall et al., 2015; Vodyanitskii and Shoba, 2015). In particular,
plant species growing in these aquatic habitats play an important role in
the cycling of trace elements because wetland plants act as the main liv-
ing collectors of trace elements (Duarte et al., 2010; Teuchies et al.,
2013). Plant communities are an integral part of the regulatory
processes occurring in wetlands and their associated food webs, conse-
quently, knowing the patterns of element accumulation and transloca-
tion in plant species and the relationship with water and sediments, is
of the utmost importance for restoring, protecting and monitoring any
aquatic ecosystem.
5. Conclusions
While the positive function of plants on element pollution remedia-
tion in wetlands is well established, other patterns involving the role of
plant ecology on trace element translocation need further investigation.
On the one hand, this study showed that wetland plants share some
general characteristics (e.g. element compartmentalization between or-
gans, bulk element concentrations in roots), on the other hand, we
found that these species tend to have a specific response in terms of
translocation and bioindication of trace elements in water and sedi-
ments. This study further corroborated the fact that accumulation and
correlation with trace elements in plants is life form independent. Con-
sequently, the patterns of element translocation cannot be easily gener-
alized in plant species because the potential of element uptake is
generally different between plants, even between congeneric species.
Acknowledgements
This study was funded by Horizon 2020 ERANET cofund WATER
WORKS 2014 – project Smart decentralised water management
through a dynamic integration of technologies – WATINTECH. This
study was financially supported also by EcoStat srl – Spin-off of Catania
University, and by the Italian Ministry of Education, University and Re-
search. The authors are thankful to all the people involved in sampling,
chemical analysis and statistical processing.
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