JES-00830; No of Pages 13
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX
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Metals and metalloid bioconcentrations in the tissues of
Typha latifolia grown in the four interconnected ponds of a
domestic landfill site
Zohra Ben Salem1 , Xavier Laffray1,2,5 , Ahmed Al-Ashoor1,3 , Habib Ayadi4 , Lotfi Aleya1,⁎
1.
2.
3.
4.
Bourgogne Franche-Comté University, Chrono-Environnement Laboratory, UMR CNRS 6249, F-25030 Besançon Cedex, France
Paris Est-Créteil University, IPE team, iEES Paris UMR 7618, F-94010 Créteil Cedex, France
Thi Qar University, IQ-64001 Al Nasiriyah, Iraq
Sfax University, LR/UR/05ES05 Biodiversity and Aquatic Ecosystem, BP 1171, CP 3000 Sfax, Tunisia
AR TIC LE I N FO
ABS TR ACT
Article history:
The uptake of metals in roots and their transfer to rhizomes and above-ground plant parts
Received 26 June 2015
(stems, leaves) of cattails (Typha latifolia L.) were studied in leachates from a domestic
Revised 15 October 2015
landfill site (Etueffont, France) and treated in a natural lagooning system. Plant parts and
Accepted 15 October 2015
corresponding water and sediment samples were taken at the inflow and outflow points
Available online xxxx
of the four ponds at the beginning and at the end of the growing season. Concentrations of
As, Cd, Cr, Cu, Fe, Mn, Ni and Zn in the different compartments were estimated and their
Keywords:
removal efficiency assessed, reaching more than 90% for Fe, Mn and Ni in spring and fall
Landfill leachate
as well in the water compartment. The above- and below-ground cattail biomass varied
Lagooning
from 0.21 to 0.85, and 0.34 to 1.24 kg dry weight/m2, respectively, the highest values
Trace elements
being recorded in the fourth pond in spring 2011. The root system was the first site of
Typha latifolia
accumulation before the rhizome, stem and leaves. The highest metal concentration was
Phytoremediation
observed in roots from cattails growing at the inflow of the system's first pond. The trend
in the average trace element concentrations in the cattail plant organs can generally
be expressed as: Fe > Mn > As > Zn > Cr > Cu > Ni > Cd for both spring and fall. While
T. latifolia removes trace elements efficiently from landfill leachates, attention should also
be paid to the negative effects of these elements on plant growth.
© 2016 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences.
Published by Elsevier B.V.
Introduction
Recent years have seen an increase in the application of
constructed wetland (CW) technology to restore water quality throughout the world, particularly in North and South
America, Asia and Europe. Presenting great ecological and
environmental advantages, with economic and social benefits as well (Herath, 2004), lagooning systems represent a
simple, eco-friendly, affordable and highly efficient biogeochemical system to collect, treat and purify waters generated
by various sources including domestic and municipal sewage, agricultural runoff, storm water and industrial discharges, as well as landfill leachate contaminated by trace
elements (Vymazal et al., 2010; Grisey and Aleya, 2016a)
which may endanger the quality of both surface waters and
groundwater (Council Directive 1999/31/EC).
⁎ Corresponding author. E-mail: [email protected] (Lotfi Aleya).
5
The two authors did equal contribution to this article.
http://dx.doi.org/10.1016/j.jes.2015.10.039
1001-0742/© 2016 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
2
J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX
Generated by waste-layer moisture and rainwater infiltrations, leachates outflowing from landfill areas are rich in
nutrients, trace elements and organic compounds which, in
turn, depend on waste material type and quantity (Kjeldsen
et al., 2002; Bichet et al., 2016). Leachate treatment in
constructed and artificial wetlands (CWs and AWs), before
discharge into the environment, partly consists of transfer of
pollutants to sediments at the bottom of the ponds via the
processes of adsorption onto suspended matter and sedimentation (Zwolsman et al., 1993). Sedimentation of polluted
particles resulting in high trace element concentrations in CW
sediments are generally considered as a sink (Hart, 1982).
Leachate treatment also consists of bioaccumulation in wetland
macrophytes (Wojciechowska and Waara, 2011). This process,
however, is heavily influenced by seasonal variations in macrophyte growth, by plant tolerance for organic, metallic and
nutrient loads, by the concentrations and mobility of elements
in the surrounding water and sediment, and also by bioavailability (Grisey et al., 2012).
Worldwide studies of emergent macrophytes have demonstrated the resistance of these species with respect to water
and sediment contents and especially to high pollution levels.
They have a capacity to accumulate and sequester elements
in below-ground (root) plant parts and to a lesser extent in
the above-ground phytomass (Bonanno, 2011). The emergent
macrophyte Typha latifolia (cattail) is one of the widely distributed, tolerant and most productive natural species in
temperate aquatic ecosystems (high biomass production and
fast growth rate) that is able to grow in harsh conditions
(Lyubenova et al., 2013). Thus, this species is commonly used
in wastewater treatment by lagooning for the removal of trace
elements (Maddison et al., 2009; Grisey et al., 2012; Kumari
and Tripathi, 2015).
Effects of metals and metalloids on components of wetland treatment areas are of particular concern at the Etueffont
landfill site (Territoire de Belfort, France), a pilot site for trace
element transfer studies in the floating, submerged and
emergent species of aquatic plants. Previous studies of the
fourth and least polluted pond of the Etueffont CW have
shown that removal through aquatic macrophyte bioaccumulation was efficient without a significant effect on cattail
growth (Grisey et al., 2012; Ben Salem et al., 2014).
The aim of the present study is to give a detailed overview over a two-season period of metal and metalloid
bioconcentration capacities of T. latifolia at the Etueffont
surface flow constructed wetland for landfill leachate treatment. Indeed, growing within the site's four interconnected
ponds, this macrophyte shows a decreasing gradient of
exposure to trace elements in both water and sediment. The
seasonal growth dynamics of T. latifolia were investigated
and trace element levels (for metals: Cd, Cr, Cu, Fe, Mn, Ni
and Zn; and for metalloids: As) in the below-ground (roots
and rhizomes) and above-ground plant parts (stems and
leaves) were determined, along with concentrations in the
corresponding water and sediment samples. The impact of
seasonal climatic conditions on trace element concentrations
in water and sediment inflow/outflow was studied and the
corresponding level in the plant's above- and below-ground
organs. This enabled us to determine the removal efficiency
of T. latifolia in water quality improvement before discharge
into the environment. Differences in metal and metalloid
concentrations in T. latifolia plant parts and translocation
properties are also discussed.
1. Materials and methods
1.1. Presentation of the study site
Covering 2.8 ha, the municipal domestic landfill of Etueffont
(Territoire de Belfort, northeastern France) was opened in
1976 in order to collect uncompacted ground household
wastes from 66 municipalities (about 50,000 inhabitants).
Solid wastes were deposited in the original cell of 20,500 m2
until 1999, and then in a new cell of 7500 m2 from 1999 to 2002.
Upon the site's closure in 2002, the layer of 200,000 tons of
accumulated crushed wastes (15 m thick) was covered by a
0.4 m thick layer of artificial soil composed of crushed organic
wastes (paper, wood, lawn cuttings, straw, fabrics) (Khattabi
et al., 2007). A drainage system was installed for downstream
leachate collection from the two cells and treatment prior to
water discharge in a nearby stream, Gros Prés Brook. The
constructed wetland (CW) is comprised of a series of four
interconnected lagooning ponds with a total area of 5250 m2.
The characteristics of the CW have been previously described
by Ben Salem et al. (2014). The water flowing through the
CW was adjusted to 59.4 m3/day during the 2011 monitoring periods with a retention time of about 87 days. The four
ponds are situated over an underlying 1 m thick layer of clay
that has a bed slope of 1%. After maintenance in the fall of 2009
(i.e., clearing and grading), the ponds were replanted with new
cattail plants (Typha latifolia L.) at a mean density of 1 m−2.
1.2. Water sampling
Three hundred thirty-six water samples were collected in
150 mL bottles from each of the four ponds, at (a) three
locations close to the inflow and (b) three locations at the
outflow, every 2 days for 2 weeks, in spring (from 04/18/2011
to 05/01/2011) and fall (from 10/17/2011 to 10/30/2011).
After collection, samples were stored at 4°C for preservation
before preparation and analysis. The samples were filtered
through a 0.45-μm membrane; 25 mL from each sample were
treated with 6 mL of 68% v/v HNO3 before analysis. Fourteen
samples of water for background values were collected in
Gros Prés Brook on the same dates (Fig. 1) and analyzed
simultaneously. Ambient environmental factors at the wetland study site, namely temperature, pH and electrical conductivity (portable multiparameter probe WTW, Multiline
P3 PH/LF-SET) were determined in situ for both sampling
campaigns.
1.3. Macrophyte and sediment sampling
Replicate samples were collected individually and processed
separately for both T. latifolia (above- and below-ground plant
parts) and sediment from three 1 m2 plots near the inflow and
outflow water collection locations of each of the four ponds:
(a) during spring growth (05/01/2011), and (b) after the summer
growth period, in late fall (10/30/2011).
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX
3
Fig. 1 – Concentrations of As, Cd, Cr and Cu (mg·(kg/DW− 1)) in sediment and water collected at inflow and outflow sampling
locations of the four ponds of the lagooning system in spring and fall 2011 (n = 6, mean ± SD). DW: dry weight.
1.3.1. Macrophytes
For the forty-eight samples, each set of roots, rhizomes, stems
and leaves was thoroughly rinsed several times with deionized water before oven drying at 80°C to a constant weight
(for about 24 hr) (Mishra et al., 2008). The dry samples were
reduced to powder in a mortar for analysis. For each plant,
a 1-g dry weight sample was digested with 3 mL HNO3 and
1 mL H2O2 at 105°C for 3 hr in a microwave digestion system,
according to the standard NF EN ISO 15587-2 (2002) before
analysis by ICP-OES (Thermofisher Scientific iCAP 6000).
1.3.2. Sediment
For the eight sampling plots, three replicate samples were
collected with a sediment corer (10 cm diameter) at about 10–
15 cm depth so as to collect both sludge deposits and a small
portion of the underlying clay. After being wet sieved through
a 5.0 mm pore-size polypropylene mesh with reagent grade
water to separate the sediment-size fraction and eliminate
plant fragments, the samples were left to settle and the water
was later decanted. The sediment clay-fractions were frozen at
−18°C, according to Annexe A of the standard NF EN 13346. After
homogenization using a mortar and pestle, and dry-sieving
through a 2.0 mm pore-size polypropylene mesh, 1 g of each
sediment sample was digested with 3 mL HNO3 and 9 mL HCl at
105°C for 3 hr in a microwave digestion system. All instruments
were cleaned before and after each sample with 10% redistilled
HNO3 and then rinsed with reagent water.
1.4. Sample analysis
The trace element concentration in water, plant and sediment samples was determined by ICP-OES (720-ES, VARIAN).
International certified reference materials for the water
(NIST-1643-e), plants (INCT-TL-1) and sediments (CRM-029)
were analyzed at the beginning and end of each batch of
samples for accuracy and precision. Instrument performance
during analysis was monitored using an internal standard.
For both macrophyte and sediment analyses, internal control
standards were analyzed with each sample and a duplicate
was run for every ten samples. The detection limits with
ICP-OES were 0.02 mg/L for As, Fe, Mn, Ni and Zn; 0.01 mg/L
for Cd, Cr and Cu. Data outputs were expressed in mg/L for
water, in mg/kg dry weight for sediment and plant materials.
1.5. Determination of phytoremediation parameters
The biological concentration factor (BCF) was calculated as the
ratio between trace element concentrations in plant material
and the concentrations in the water to which the macrophyte
is exposed (Zayed et al., 1998). This index defines the ability
of T. latifolia to uptake metals and metalloids with respect to
concentrations in the surrounding waters of the lagooning
system's different ponds.
The translocation properties of T. latifolia are described as
ratios of trace elements in sediment to those of the above- and
below-ground plant parts and are expressed in the Enrichment
coefficient (EC) given in the four following equations (Sasmaz
and Sasmaz, 2009): ECR = Croot / Csediment; ECRh = Crhizome /
Csediment; ECS = Cstem / Csediment; ECL = Cleaf / Csediment.
The translocation factor (TLF) was calculated as element
concentration ratio of plant leaf to plant roots and is given
in the equation as Cleaf / Croot (Sasmaz and Sasmaz, 2009).
The Leaf-Stem Ratio (LSR) was also calculated as the fraction
of Cleaf / Cstem.
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
4
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The biological concentration factor (BCF) as well as enrichment coefficient (EC) and the transfer factor (TLF) were
calculated only for those elements detected in water, sediment and plant organs.
1.6. Statistical analysis
Before conducting any statistical analysis, normality of the
data was checked with a Kolmogorov–Smirnov (KS) test.
Statistical differences between inflow and outflow trace
element concentrations in the four ponds were assessed
using a mean comparison test (p < 0.05). Also, bioaccumulation and translocation factors determined for the four ponds
during the two sampling periods were statistically analyzed
using a multifactor analysis of variance (ANOVA); differences
among mean values were evaluated by Tukey's post-test
when appropriate. In all tests, a significance level of p < 0.05
was used for differences in critical values. A linear regression model was used to evaluate the effect of trace element
concentration in the water solutions on the mean concentration in T. latifolia plant part biomass. All statistical
analyses were performed with R statistical analysis system
(www.R-project.org).
2. Results
2.1. In-/outflowing water quality
2.1.1. Ambient environmental factors
From pond to pond, pH did not vary noticeably during the
experiment (Table 1). Though it increased in spring, with the
highest values recorded at inflow of pond 3 (8.1), no significant
seasonal variations were recorded for any pond. For the two
sampling periods, water temperature at pond 1 inflow showed
generally higher values than those found in the remaining
three ponds. However, no significant differences were recorded for any of the system's ponds (neither at inflow nor
outflow). The highest temperature was recorded in spring in
pond 1 (11.2°C), but without significant variations between
inflow and outflow. The water in the lagooning system cooled
during fall, though freezing conditions never occurred during
the study period; the lowest temperature was recorded at
pond 4 outflow (4.6°C).
Electrical conductivity in water varied from spring to fall
with the highest values recorded in spring at pond 1 inflow.
Conductivity for both seasons was significantly reduced in
ponds 2, 3 and 4 compared to pond 1, with less than 1250 μS/cm
at both in- and outflow (Table 1). The mean dissolved oxygen
(DO) concentration of water flowing through the system was
not significantly different between ponds during the 2 sampling
periods. However, high DO values were recorded at pond 1
inflow, with the highest DO measured in spring (Table 1).
2.1.2. Metals and metalloids in water
In-/outflow of the four ponds, and Gros Prés Brook samples
were analyzed for metal and metalloid content (As, Cd, Cr, Cu,
Fe, Mn, Ni and Zn) (Figs. 1 and 2). Background trace element
concentrations from samples collected in Gros Prés Brook
were close to or under the detection limits of the ICP-OES
(data not shown). Mean concentrations of As, Cd and Cr in
water samples collected at both in- and outflow of the four
ponds was generally constant for the two seasons, remaining
below detection limit values throughout the experiment.
Seasonal decreases in trace element content were recorded
at in −/outflow in all four ponds with a peak in spring for Cu,
Fe, Mn, Ni and Zn (Figs. 1 and 2). While significant reductions
(p < 0.01) were recorded for Zn in all of the ponds, only Cu and
Fe were significantly reduced compared to the concentrations
measured in ponds 1 to 3 in spring. Mn and Ni levels were
significantly reduced (p < 0.01) in comparison to the concentrations measured for spring and fall in ponds 1 and 2 only
(Figs. 1 and 2).
For both sampling seasons significant decreases in concentrations in inflow and outflow waters of the first three ponds
were observed for Fe, Mn, Ni and Zn only. Concentrations of Cu
recorded in in-/outflow waters were significantly reduced for
the two sampling periods in ponds 1 and 2 only. Significant
trace element concentration removal in the Etueffont treatment
system was recorded during both sampling periods (As, Cd
and Cr excepted). In-/outflow trace element removal in water
flowing through the entire system varied from −17% to −94% in
spring and from −83% to −95% in fall, with a global efficiency
up to 90% for Fe, Mn and Ni (Zn in fall 2011 only). Cu removal
efficiency ranged from 83 to 88%.
2.1.3. Metals and metalloids in sediments
Data recorded during the two sampling periods in the four
ponds are shown in Figs. 1 and 2. For both spring and fall
significant decreases in concentrations at inflow and outflow
of the first three ponds were observed for As, Cd, Cr, Fe and
Zn. However, no significant temporal differences were recorded for Cu or Ni (at inflow or outflow), or Mn (ponds 1 and
2 only). In pond 4, in contrast, significant seasonal decreases
Table 1 – Morphometric and physical characteristics of the four interconnected ponds of the Etueffont lagooning system.
Etueffont interconnected ponds
Pond 1
Temperature (°C)
pH
Conductivity (μS)
DO (mg/L)
Spring
Fall
Spring
Fall
Spring
Fall
Spring
Fall
10.4
6.4
7.6
7.7
1792.1
1687.6
6.84
7.68
±
±
±
±
±
±
±
±
0.6
0.5
0.1
0.2
124.2
86.4
3.29
2.67
Pond 2
10.3
6.1
7.8
7.8
1245.3
952.9
5.23
7.82
±
±
±
±
±
±
±
±
0.2
0.3
0.1
0.1
38.4
14.9
1.04
0.76
Pond 3
9.8
5.7
7.9
7.8
1027.7
826.4
5.79
6.38
±
±
±
±
±
±
±
±
0.2
0.4
0.2
0.1
23.7
16.8
0.84
0.48
Pond 4
9.7
5.2
7.6
7.7
1057.0
756.8
6.73
5.18
±
±
±
±
±
±
±
±
0.3
0.4
0.1
0.1
13.2
37.9
1.24
1.32
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
5
Fig. 2 – Concentrations of Fe, Mn, Ni and Zn (mg·(kg/DW−1)) in sediment and water collected at inflow and outflow sampling locations of the four ponds of the lagooning system
in spring and fall 2011 (n = 6, mean ± SD).
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
6
J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX
in metal concentrations at inflow and outflow were observed
for Cd, Cr, Cu, Mn and Zn only. Moreover, no significant
temporal differences were recorded for Fe and Ni (at inflow
and outflow) (Fig. 2), or for As (at outflow only) (Fig. 1).
Trace element content in outflow sediment showed
generally lower values than those found at inflow (Cu and
Ni except in pond 1). In-/outflow trace element removal in
sediment varied from − 2% to ˗61% in spring and from − 6%
to − 62% in fall. Only Zn was significantly reduced (p < 0.05)
compared to the concentration measured at inflow, whatever
the pond or sampling month. For As, Cr and Fe, concentrations* were also significantly reduced between inflow and
outflow, in both seasons but only in ponds 1 to 3. Mn levels
were significantly reduced in ponds 2 and 3 only. No significant removal was recorded for Ni. Cd was significantly
reduced (p < 0.05) compared to the concentrations measured
at inflow for spring and fall in ponds 3 and 4. Significant
removal of metal and metalloid contents was recorded in all
ponds during both sampling periods (Cu and Ni excepted)
with a global efficiency of less than 60% for Cd, Cr, Cu, Mn and
Ni in spring and fall, but of up to 90% for As in sediment.
2.2. Biological variables
2.2.1. Macrophyte phytomass
The average values of above- and below-ground cattail
biomass harvested during the two study months in the four
ponds are shown in Fig. 3. The below-ground plant part (roots
and rhizomes) biomass varied from 0.34 to 1.24 kg DW/m2,
the highest value being measured at pond 4 outflow in spring
and the lowest at pond 1 outflow in fall.
T. latifolia was found to be similar in terms of above-ground
biomass (stems and leaves) in ponds 2, 3 and 4 where they grow
(Fig. 3) without significant differences between inflow and
outflow sampling points (0.56 ± 0.14 and 0.49 ± 0.16 kg DW/m2
in spring and fall, respectively). The highest shoot biomass
was measured at pond 4 inflow in fall, with 0.85 kg DW/m2.
The lowest above-ground macrophyte biomass was recorded
in cattails collected at pond 1 inflow for the same sampling
period (0.21 kg DW/m2).
No significant difference was observed in above- and
below-ground plant biomass nor in relation to the sampling
location within ponds 2, 3 and 4, comforting the hypothesis
of uniform growing conditions for the plants. However, in
comparing the system's first and last ponds, contrasting
data were observed at the beginning and the end of the
growing season for both above- and below-ground biomass of
T. latifolia. Moreover, cattail total biomass generally decreased
in ponds 1 and 2 in spring and fall, but without significant
differences between any of the four ponds for spring. A
significant difference in biomass was observed for emergent
macrophytes collected at pond 1 inflow only.
Fig. 3 – Above and below-ground biomass (kg·(DW/m−2)) of
T. latifolia sampled at inflow and outflow of the four
interconnected ponds in spring and fall 2011
(n = 6, mean ± SD).
2.2.2.1. Below-ground plant parts: Roots. Except for As, B, Cd,
Fe and Cu, significant differences in all metal concentrations
between the two sampling periods were recorded for roots
(p < 0.05), whatever the pond (Figs. 4 and 5). The highest metal
concentrations in T. latifolia were found for Fe and Mn in roots
on the inflow side of the first pond in spring with 71,196
and 14,939 mg/kg DW, respectively. Whatever the season
and the sampling location, the lowest metal concentrations
were recorded for Cd in roots with less than 3.19 mg/kg DW
(data not shown). In cattail roots, the average metal and
metalloid concentrations in the four ponds can be ranked
as follows: Fe > Mn > As > Zn > Cr > Cu > Ni > Cd for the two
sampling periods.
2.2.2. Metal and metalloid storage in macrophytes and
relationships with sediment
2.2.2.2. Below-ground plant parts: Rhizomes. Only Cd and Cr
did not vary significantly with season in T. latifolia rhizomes,
neither at inflow nor outflow (Figs. 4 and 5) (except for Cr
at pond 4 inflow). Whatever the pond and the harvesting
date, Cd in T. latifolia rhizome remained below the detection
limits (BDL). The highest metal concentrations in T. latifolia
were generally found for Fe and Mn in spring in rhizomes
collected on the inflow side of pond 1 with 20,203 and 3104 mg
per kilogram DW, respectively. Moreover, no significant variations in rhizome were recorded for Cu between the two
periods at pond 4 outflow. Except for pond 1, the trend
in the average metal concentrations in cattail stems was:
Fe > Mn > Zn > As > Cu > Ni > Cr for the two sampling periods.
Concentrations measured in T. latifolia during the two
sampling periods are shown in Figs. 4 and 5. In most cases,
trace element concentrations were significantly higher in
roots and rhizomes than in leaves and stems of the T. latifolia
growing at both inflow and outflow.
2.2.2.3. Above-ground plant parts: Stems. As, Cd and Cr
in stems remained below the detection limits (BDL) in the
T. latifolia stems harvested from all ponds, regardless of
collection time (Figs. 4 and 5). Significant differences from
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX
7
Fig. 4 – Concentrations of As–Cr, Cd, Cu and Fe (mg·(kg/DW−1)) in above and below-ground biomass (kg·(DW/m−2)) of T. latifolia
collected at inflow and outflow sampling locations of the four ponds of the lagooning system in spring (S) and fall (F) 2011
(n = 6, mean ± SD).
pond to pond between the two sampling periods were
recorded for Fe and Zn only (p < 0.05). The highest metal concentrations in T. latifolia were found for Fe and Mn in stems at
pond 1 inflow in spring with 1438.7 and 1669.4 mg/kg DW,
respectively. The same general trend as in cattail stems was
observed in leaves with: Mn > Fe > Zn > Cu > Ni for the two
Fig. 5 – Concentrations of Mn, Ni and Zn (mg·(kg/DW−1)) in above and below-ground biomass (kg·(DW/m−2)) of T. latifolia
collected at inflow and outflow sampling locations of the four ponds of the lagooning system in spring (S) and fall (F) 2011
(n = 6, mean ± SD).
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
8
J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX
sampling periods (As, Cd and Cr remaining below the
detection limits).
and Cd were not analyzed in the water, since concentrations
were below the method's detection limit, preventing calculation of their BCF.
The mean calculated ECR (Table 2) varied from 0.19 to 4.39.
Mean ECR values decreased in the following order: Zn < Cu <
Cr < Ni < Fe < Cd < Mn < As. The highest ECR values reported
were for As in pond 3 (in spring) and Mn in pond 4 (in both
spring and fall). Except for As and Mn, the ECR of T. latifolia
were below 1.0 for all of the studied metals and metalloids,
whatever the pond or sampling period (Table 2).
The mean enrichment coefficients for rhizomes (ECRh)
(Table 2) ranged from 0.02 to 0.57, the highest values being
measured for Mn in spring (in pond 1). For As and Fe the
highest ECRh values were observed also observed in spring
only in both ponds 1 and 2. The rhizome enrichment coefficients were from 71% to 98% lower than those found in the
roots, with the decrease in elements as follows: Zn < Fe <
Cu < Ni < Mn < As < Cr (Cd not evaluated (BDL)). Enrichment
coefficients for all analyzed elements were below 1.
2.2.2.4. Above-ground plant parts: Leaves. The same pattern
was observed among both stems and leaves for As, Cd and Cr
with concentrations remaining below the detection limits,
regardless of collection time (Figs. 4 and 5). As in roots and
rhizomes, trace element concentrations in above-ground plant
parts were maximal in spring after plant growth, whereas a
general decrease occurred in fall with senescence. With the
exception of the four elements, trace element uptake by T. latifolia
above-ground phytomass (stems and leaves) showed similar
significant seasonal variations to those of below-ground plant
parts at inflow and outflow in all four ponds. Significant
differences either at inflow or outflow in the four lagooning
ponds between the two sampling periods were recorded for Mn
only (p < 0.05). The highest metal concentrations for Fe and Mn
in T. latifolia were found in stems at pond 1 inflow in spring with
571.6 and 4011.8 mg/kg DW, respectively. Except for pond 1, the
trend in the average metal and metalloid concentrations in the
cattail rhizomes was as follows: Mn > Fe > Zn > Cu > Ni for the
two sampling periods (As, Cd and Cr below the detection limits).
2.2.3.1. ECS/ECL. The mean enrichment coefficients for
stems (ECS) and leaves (ECL) ranged from 0.00 to 0.39 and
from 0.00 to 0.88, respectively (Table 3). For Mn, the highest
ECS and ECL values were observed in pond 1 in both spring
and fall. The mean decrease in ECS and ECL values was as
follows: Fe < Cu < Ni < Zn < Mn and Fe < Zn < Ni < Cu < Mn,
respectively. EC was not evaluated for As, Cd and Cr since
concentrations remained below detection limits for both
sampling periods. Except for Mn in leaves of T. latifolia
collected at inflow of ponds 1 and 3 (spring), enrichment
coefficients for all analyzed elements were below 1.
2.2.3. Biological concentration factor (BCF) and enrichment
coefficient (ECR)
The ability index of T. latifolia to uptake trace elements from
water (BCF) for collected plants at inflow and outflow of the
four ponds is summarized in Table 2. Mean values of BCF
increased according to element as follows: Ni < Zn < Cr <
Cu < Mn < Fe. The highest BCF values determined were for Fe
and Mn (in both spring and fall) in pond 4. The elements As
Table 2 – Biological concentration factor (mean ± SD), enrichment coefficient (for roots and rhizomes) of T. latifolia from the
four ponds of the Etueffont lagooning system.
As
Cd
Cr
Cu
Fe
Mn
Ni
Zn
BCF
ECR
ECRh
Spring 2011
Spring 2011
Spring 2011
Pond 1
Pond 2
Pond 3
Pond 4
Pond 1
Pond 2
Pond 3
Pond 4
Pond 1
Pond 2
Pond 3
Pond 4
ne
ne
5014
796
50,052
19,262
343
1074
ne
ne
ne
1495
70,623
36,956
539
1230
ne
ne
ne
2062
107,273
80,529
1339
1284
ne
ne
ne
3453
208,297
120,638
2002
1337
2.73
0.86
0.91
0.44
0.55
3.57
1.15
0.45
3.54
0.66
0.93
0.32
0.73
3.49
0.9
0.47
4.39
0.59
0.92
0.32
0.84
3.79
0.92
0.40
3.58
0.64
0.60
0.33
0.72
4.04
0.9
0.39
0.16
ne
0.02
0.09
0.16
0.57
0.17
0.07
0.25
ne
0.02
0.04
0.21
0.29
0.12
0.06
0.22
ne
0.02
0.04
0.17
0.36
0.09
0.06
0.16
ne
0.02
0.03
0.05
0.29
0.06
0.08
Fall 2011
As
Cd
Cr
Cu
Fe
Mn
Ni
Zn
Fall 2011
Fall 2011
Pond 1
Pond 2
Pond 3
Pond 4
Pond 1
Pond 2
Pond 3
Pond 4
Pond 1
Pond 2
Pond 3
Pond 4
ne
ne
ne
974
41,050
11,890
149
721
ne
ne
ne
1814
67,997
21,662
193
823
ne
ne
ne
2311
185,209
46,058
432
807
ne
ne
ne
2043
317,154
62,687
782
4592
1.33
1.06
0.25
0.46
0.53
1.46
0.41
0.23
2.5
0.9
0.3
0.33
0.78
1.25
0.33
0.19
2.49
0.60
0.29
0.31
0.77
1.74
0.30
0.19
3.78
0.86
0.21
0.36
0.67
2.18
0.29
0.3
0.07
ne
0.02
0.07
0.05
0.13
0.03
0.04
0.13
ne
0.02
0.04
0.06
0.09
0.02
0.04
0.15
ne
ne
0.03
0.05
0.12
ne
0.05
0.09
ne
ne
0.04
0.02
0.17
0.03
0.08
BCF: biological concentration factor; EC: enrichment coefficient; ECRh: enrichment coefficients for rhizomes.
ECR = Croot / Csediment; ECRh = Crhizome / Csediment.
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
9
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX
Table 3 – Enrichment coefficient (for stems and leaves), leaf/stem ratio and Transfer Factor (leaf/root) of T. latifolia from the
four ponds of the Etueffont lagooning system.
ECS
ECL
LSR
TLF
Spring 2011
Spring 2011
Spring 2011
Spring 2011
Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2 Pond 3 Pond 4
Cu
Fe
Mn
Ni
Zn
0.03
0.01
0.35
0.04
0.09
0.02
0.01
0.29
0.03
0.08
0.02
0.01
0.32
0.03
0.08
0.02
0.00
0.38
0.03
0.09
0.03
0.01
0.88
0.03
0.02
Fall 2011
0.02
0.01
0.81
0.02
0.01
0.01
0.01
0.87
0.02
0.00
0.03
0.00
0.77
0.02
ne
0.78
0.77
2.52
0.86
0.29
Fall 2011
1.09
0.96
2.85
0.75
0.12
0.91
1.02
2.67
0.91
0.05
1.54
1.10
2.02
0.93
0.04
0.06
0.01
0.25
0.03
0.05
Fall 2011
0.06
0.01
0.23
0.03
0.02
0.04
0.01
0.23
0.03
0.01
0.09
0.00
0.19
0.03
ne
Fall 2011
Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2 Pond 3 Pond 4
Cu
Fe
Mn
Ni
Zn
0.02
0.00
0.39
Ne
0.05
0.01
0.00
0.29
ne
0.06
0.01
0.00
0.37
Ne
0.06
0.02
0.00
0.33
Ne
0.07
0.03
0.00
0.75
0.02
0.02
0.02
0.00
0.48
0.02
0.01
0.03
0.00
0.59
0.03
0.00
0.03
0.00
0.41
0.03
ne
1.61
1.61
1.87
1.01
0.35
1.51
1.78
1.63
ne
0.15
1.64
2.77
1.61
ne
0.09
1.70
2.81
1.13
ne
0.09
0.06
0.01
0.51
0.06
0.08
0.05
0.00
0.38
ne
0.05
0.10
0.01
0.34
ne
0.03
0.09
0.00
0.19
ne
ne
Not evaluated for As, Cd and Cr (below detection limits) whatever the pond of the system. ECS: enrichment coefficients for stems; ECL:
enrichment coefficients for leaves; LSR: Leaf-Stem Ratio.
ECS = Cstem / Csediment; ECL = Cleaf / Csediment; LSR = Cleaf / Cstem; TLF = Cleaf / Croot.
All results are expressed as positive linear correlations
between trace element concentrations in water (or sediment)
and the different plant organs (root, rhizome, stem and leaf)
(data not shown).
2.2.4. Transfer factor (LSR and TLF)
The transfer factor was used in order to determine for the two
sampling periods the ability of T. latifolia to transfer trace
elements from roots to shoots (stems) (TLF) as well as from
stem to leaves (LSR) in the specific conditions that exist in the
four interconnected ponds of the Etueffont lagooning system.
The calculated TLF and LSR of T. latifolia in the four ponds
are summarized in Table 3. The highest leaf/stem ratio was
observed for Mn with mean LSR ranging from 2.02 to 2.85 and
from 1.13 to 1.87 for spring and fall, respectively. High LSR
have also been determined for 2 other metals with mean
values ranging from 0.78 to 1.7, and 0.77 to 2.81 for Cu and
Fe, respectively (all sampling dates taken into account) (not
evaluated for As, Cd and Cr).
The mean TLF for T. latifolia varied from 0.00 to 0.23 and
from 0.00 to 0.51 in spring and fall, respectively, (all ponds
considered), its exclusion capacity found to be: Fe < Ni <
Zn < Cu < Mn (Not evaluated for As, Cd and Cr).
reported for natural stands in the north central United States
by Pratt et al. (1984) (4.3–14 t DW/ha) and were in accordance
with biomass values measured by Maddison et al. (2009,
Estonia). Though above-ground biomass of T. latifolia collected
in the Etueffont CW was generally greater than that reported
by Atkinson et al. (2010) in temperate freshwater marshes in
southwestern Virginia (USA), the biomass of cattail samples
from pond 1 at Etueffont remained lower compared to that
recorded by Atkinson et al. (2010) in freshwater ecosystems.
Observations in the cattail population in natural and constructed wetlands reported in the literature indicate that trace
element concentrations in the sediment in Etueffont's ponds
2, 3 and 4 did not significantly affect T. latifolia growth, while
in pond 1 they had a stunting effect. On the contrary, the high
concentrations of metals recorded at pond 1 inflow led to a
significant reduction in macrophyte development (maximum
length of fully expanded leaves, number of leaves, length of
stems, etc.) as well as in the total phytomass of the studied
cattails. Growth reduction along with the increasing trace
element concentrations in both sediment and water are
positively correlated to the reduction of the BCF for Cu, Fe,
Mn, Ni and Zn of the macrophytes growing in all four of the
system's ponds, and also to the ECR reduction of Fe and Mn
(the two most concentrated elements in the sediment).
3. Discussion
3.2. Water and sediment analyses
3.1. Metals and metalloids and macrophyte phytomass
3.2.1. Water analysis
In the present study of the four interconnected ponds of
the Etueffont lagooning system, T. latifolia attained the highest
below-ground biomass at pond 4 outflow in spring (at pond
4 inflow for above-ground biomass). The mean biomass of
aerial parts of T. latifolia, recorded in ponds 2, 3 and 4 (ranging
from 0.48 ± 0.14 to 0.61 ± 0.12 to kg DW/m2) in both spring
and fall, were within the same range of above-ground yields
Concentrations of Cu, Fe and Zn in water passing through
ponds 1 to 3 of the Etueffont lagooning system varied notably
during the two study seasons (p < 0.05). Variations in concentrations of these five elements in all four interconnected
ponds decreased along the water flow path. However, in
pond 4 (before discharge into Gros Prés Brook), a significant
seasonal inflow/outflow decrease was recorded only for Fe
and Zn (in spring) and Mn (in fall). For As, Cd and Cr, the
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
10
J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX
concentrations in the water entering the system remained
below the detection limits during the study period. The
observed concentrations of elements in the water entering
the Etueffont system were in the same range as in the
leachates from mixed municipal solid waste landfills reported
by Kjeldsen et al. (2002) in a wide range of studies or those
found by Justin and Zupančič (2009) from a CW with six
interconnected ponds designed for landfill leachate pretreatment (Slovenia). However, data collected at the Etueffont
CW inflow were generally higher than (for Cd, Cr, Cu, Mn,
Ni, Zn) or similar to (for Fe) observations usually reported for
domestic wastewater or landfill leachate treatment systems
(Peverly et al., 1995). Moreover, metal concentrations were
higher in spring than in fall, whatever the pond, corroborating
the results of Grisey et al. (2012) observed in the fourth pond
of the same experimental site. These increases may result
from the increased spring rainfall which leads to increased
rainwater infiltrations, waste-layer moisture and lixiviation
(Khattabi et al., 2007; Grisey and Aleya, 2016b). The element
concentrations may also be removed less efficiently from
water flowing through the system due to a reduced fixation
during winter and early spring due to low or total absence of
biological activity.
3.2.2. Sediment analysis
Metal concentrations in the sediments collected from the four
Etueffont ponds were similar (for Ni) or higher than (for Cd, Cu
and Zn) the typical ranges of metal concentrations measured
in bottom sediments considered by Bowman and Harlock
(1998) to be European background values (expressed in mg/kg:
Cd 0.1–1, Cu 2–100, Ni 0.5–100, Zn 10–200). Except for Cd and
Cr, metals and metalloids in the Etueffont sediment generally
exceeded the freshwater sediment quality guidelines determined by MacDonald et al. (2000) in their evaluation of
sediment chemistry concentrations.
Compared to data measured in the horizontal or vertical
subsurface flow of constructed wetlands studied by
Samecka-Cymerman et al. (2004), the sediments in the four
Etueffont ponds were generally more contaminated, showing
higher concentrations of Cd, Cu, Fe, Mn and Zn. Moreover, the
present study reported very similar (Ni) or higher (Cd, Cu, Mn
and Zn) concentrations of elements when compared to the
values recorded by Sasmaz et al. (2008) in Kehli Stream
(Elazig, Turkey).
As for water, trace element concentrations in sediment
samples collected at Etueffont showed higher values in spring
than in fall. As reported by Goulet and Pick (2001), the spring
peak in sediment could be the result of increased input, but
also of a lower photosynthesis rate of macrophytes in the
system impacting element uptake. Moreover, the reductive
dissolution/oxidative reprecipitation cycle of redox sensible
elements such as Fe and Mn may affect speciation which
largely controls element bioavailability of other metals.
Thus, increased concentration of Fe or Mn in spring is induced
when these elements are dissolved to particulate phases
in metal transformations in suboxic and anoxic conditions
(low microbial respiration) (Zaaboub et al., 2014). The decrease
observed in intermediate redox conditions in fall is caused by
reoxygenation and a release of these elements into the water
flowing through the system.
3.3. Root and rhizome metal and metalloid storage from water
and sediments
Analysis of the macrophytes growing at inflow/outflow of the
four ponds indicated that Fe and Mn were the two most
concentrated elements in below-ground plant parts (roots and
rhizomes) of T. latifolia (more effectively in spring than in fall).
Though not always similar, depending on the specific wetland
and climatic conditions, the values are in accordance with
those reported by Sasmaz et al. (2008) for Cu, Mn, Ni, and Zn
from T. latifolia in a Turkish stream, but higher values were
observed for Cd and Mn in the Etueffont system. Furthermore,
Cu and Zn concentrations measured in Etueffont T. latifolia
below-ground organs are similar to those reported in cattails
from Estonian wetlands by Maddison et al. (2009), but higher
than those observed by Tanner (1996) in New Zealand or by
Klink et al. (2013) in Poland. Moreover, the levels of Cr in
cattails from the Etueffont ponds were generally similar to
values reported for the less polluted sites of the Mexican
Tanque Tenorio artificial wetland (Carranza-Álvarez et al., 2008).
However, average concentrations of Fe and Mn at Etueffont
were generally higher than those reported (Carranza-Álvarez
et al., 2008; Klink et al., 2013) for cattail roots growing in many
constructed wetlands.
The roots of macrophytes such as T. latifolia act as filters
in order to avoid the potential toxic effects induced by high
element concentration in above-ground plant tissues. Thus,
though toxic elements such as Cd, Cr and Ni (with Cu and Zn
to a lesser extent) were highly concentrated in the surrounding sediment, uptake and accumulation of these metals in
below-ground plants parts were limited with a lower uptake
achieved in rhizomes compared to roots (mean ECR: 0.19 to
1.15; mean ECRh: from 0.01 to 0.04). Observations on cattail
roots are in accordance with Ahmad et al. (2010) and Klink
et al. (2013), who demonstrated the bioaccumulation capacity
of these tissue associated with a strong ability to limit rootshoot transfer developed by metal tolerant species (supported
by low ECL and TLFs values below 0.1), most likely due to
inefficient metal transport systems (Zhao et al., 2002). The
limitation of transfer towards and bioaccumulation in rhizomes and above-ground plant parts (stems and leaves),
characteristic of excluding species (Peverly et al., 1995; Weis
and Weis, 2004) is in opposition to facilitated uptake and
translocation of metals as observed in hyper accumulator
plants. This accumulation in roots by most vascular macrophytes is strongly related to the low selectivity for metals
present in the surrounding environment due to the lacunar
system of large intercellular air spaces of the cortex parenchyma (Sawidis et al., 1995).
In addition, elements involved in photosynthetic processes
such as Mn and Fe, are efficiently absorbed by plant roots
(mean ECR: from 0.53 to 0.84 and from 1.25 to 4.04 for Fe and
Mn, respectively) whatever the pond. However, root systems
do exert a strong selection since scarcely any Fe and Mn were
transferred from root to rhizome, as indicated by low ECRh
values for most metals (mean ECRh: from 0.02 to 0.16 and
from 0.09 to 0.57 for Fe and Mn, respectively).
Thus, in accordance with results previously described in
the literature, element concentrations observed in the welldeveloped root system of most vascular macrophytes appear
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX
to reflect the fact that higher metal concentrations are
generally to be found in surrounding sediment than is usually
the case in wetland waters where they remain at low levels
(Sawidis et al., 1995). This also supports results described by
Deng et al. (2004) and Aksoy et al. (2005) who postulated
that elements taken up by rooted helophytes and stored in
below-ground organs were mainly sediment derived. However, the route of exposure (and bioavailability) depends
mainly on water/sediment metal exchange and element
interaction, which are affected by the environmental characteristics of water and sediment (Temperature (°C), Oxidation
Reduction Potential (ORP), pH, water ion content, and salinity
conditions) (Larsen and Schierup, 1981; Schierup and Larsen,
1981).
3.4. Aerial parts storage and leaf to root plant ratio (TLF)
Mean concentrations of most metals and metalloids in the
stem and leaf parts of T. latifolia growing in ponds 1 to 3 were
found to be higher (for Fe, Mn, Zn) or within the same range
(for Cu, Cd and Ni) of values given for stems and leaves of
T. latifolia growing in Polish ponds (Klink et al., 2013). Except
for Mn, metal concentrations in T. latifolia stems and leaves
were lower than those reported by Sasmaz et al. (2008)
(Turkey). Though values of Cd, Cu and Zn similar to those
reported by Maddison et al. (2009) (Estonia) were recorded for
leaves from Etueffont, greater concentrations were observed
for Zn in stems (except in fall in pond 4). Concentrations
of these elements during the present study remained below
the threshold values for plants (Cu: 20–100 mg/kg; Zn: 100–
400 mg/kg), whatever the sampling pond or period.
For Fe and Mn, average concentrations in above-ground
organs from cattails sampled in the Etueffont ponds were
generally in the same range of values as those found for
the same species collected in the Mexican Tanque Tenorio
artificial wetland (Carranza-Álvarez et al., 2008), but represented twice (i.e., 40–500 mg/kg) or six times (i.e., 5–200 mg/kg)
higher than values considered as phytotoxic by Allen (1989)
and Markert (1992), respectively. Likewise, Mn concentrations
recorded in the Etueffont ponds exceeded the threshold
values defined by Allen (1989) and Markert (1992) (300–500
and 30–700 mg/kg, respectively) as toxic for plants, surpassing
the harmful effect limits reported by Pais and Jones (2000).
These two elements are directly or indirectly involved as
promoters (or inhibitors, such as Mn in the case of chlorophyll
biosynthesis) in many biological processes including photosynthesis, respiration, redox enzymatic processes, photochemical nitrate and nitrite reduction, N2 fixation, nitrogen
metabolism and carbohydrate utilization (Pais and Jones,
2000; Memon et al., 2001; Carranza-Álvarez et al., 2008).
The transfer factor (TLF) generally showed low transport of
elements from roots to shoots (Table 3), not exceeding 1.
Uptake and bioaccumulation of Cu, Fe, Ni and Zn in aboveground tissues (both stems and leaves) were very limited (ECS
and ECL < 0.2), indicating the inefficient translocating action
from the root and rhizome system to the aerial plant parts.
This relative immobilization of metals in the root system is
verified by the determined TLF, which underlines the excluding behavior of the studied macrophyte as a metallophyte
species (Bonanno, 2011; Klink et al., 2013). However, some
11
elements are less immobilized in below-ground organs as
shown by their increased ECS, ECL and TLF values. Thus,
though Fe was sequestred in below-ground plant parts, Mn
was more easily transported than other elements and was
heavily concentrated in leaves of T. latifolia sampled at inflow
as well as at outflow of all four of the interconnected Etueffont
ponds (mean ECL and TLF: from 0.41 to 0.88 and from 0.19 to
0.51, respectively). The same results were observed by Sasmaz
et al. (2008) with TLF values ranging from 0.39 to 1.18. These
results are also in accordance with the observations of Klink
et al. (2013) assuming leaves to be the second storage site after
the root system for Mn.
Thus, the excluding ability of T. latifolia under the conditions of the Etueffont CW was as follows: Mn > Cu > Ni >
Zn > Al > Fe (not evaluated for As, Cd, Cr).
With the exception of Cu (increased in pond 4), no significant differences in transfer factor were observed between
ponds in spring 2011. For fall 2011, significant variations were
observed with increasing TLF for Cu, decreasing for Fe and Mn
with the decreasing concentrations of elements in the four
ponds.
Lower concentration of metals observed in stems and
leaves than in roots may be related to protective mechanisms
developed by tolerant plants to cope with metal stress
induced by surrounding water and sediment, and to prevent
toxic elements from penetrating into above-ground organs
so as to avoid deleterious effects on metabolism and photosynthesis (Peverly et al., 1995). This sequestration process
may result from the physical absorption of potentially toxic
elements at extracellular negatively charged sites in the
root-cell wall of cattails (cell wall-bound fraction) (Mangabeira
et al., 1999). However, metal sequestration of phytotoxic
elements as well as the translocation of essential elements
from below- to above-ground plant parts may be affected by
conflicting and synergetic inter-element processes. Seasonal
plant growth dynamics (season-dependent physiology) and
seasonal storage and detoxification ability may also greatly
influence metal transport between the different plant organs
(Mishra et al., 2008). On the other hand, though essential
as oligoelements for plant metabolism and abundantly
translocated from roots into above-ground tissues for metabolic use, elements such as Cu, Fe, Mn and Zn needed as
metabolism cofactors may produce adverse effects if concentrations exceed threshold limit values in plant tissues.
Thus, plants heavily exposed to metals present important
alterations in their photosynthetic processes (Baszynski
et al., 1980; Memon et al., 2001), affecting the photosynthetic
electron transport (Siedliecka and Baszynski, 1993), photophosphorylation (Baszynski et al., 1980), carbon fixation
capacity (Bienfait, 1988), carbohydrate metabolism (Borkert
et al., 1998) and enzyme activity or protein function (Bonanno
and Lo Giudice, 2010).
High concentrations of both essential and toxic elements
have been shown to affect photosynthetic pigment synthesis
and degradation (Stiborova et al., 1986) and chloroplast
ultrastructure (Stoyanova and Chakalova, 1990). Disturbances
in nutrient uptake and sulfate assimilation (Baszynski et al.,
1980), water balance (due to alteration of plasma membrane
properties) (Sanità di Toppi and Gabbrielli, 1999), root growth
and proliferation (Šottníková et al., 2003) have also been
Please cite this article as: Ben Salem, Z., et al., Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the
four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039
12
J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX
described in the literature as metal concentrations surpassed
critical values. Thus, most of the Mn (along with other
elements translocated to above-ground plant parts) is probably concentrated in a non-toxic form in the cell walls of
the epidermis, collenchyma, bundle sheath cells, and in a
leaf vacuolar compartment and apoplast, away from metabolically active compartments, e.g., cytosol, mitochondria and
chloroplast, as reported by Memon et al. (1981).
Defined as a metal tolerance strategy so as to protect aerial
plant parts from metal-induced injuries, sequestration processes in T. latifolia have also been demonstrated for Cd
(Taylor and Crowder, 1983) and Zn (Klink et al., 2013).
4. Conclusions
Removal of toxic elements via the process of aquatic macrophyte bioaccumulation was analyzed in the four interconnected ponds of the Etueffont lagooning system. Trace element
concentrations in water and sediments as well as in above- and
below-ground plant parts of T. latifolia were examined. Results
show that constructed wetland systems can effectively treat
landfill leachates to achieve high quality effluent that can
be discharged into the environment without danger to either
surface water or groundwater. Concentrations of Fe, Mn, Ni and
Zn in water were significantly reduced in ponds 1 to 3 for the
two studied seasons, the maximum reduction being observed
for iron in pond 3 in fall 2011 (−80%).
Concentrations of the studied metals in T. latifolia plant
tissues generally decreased as follows: roots > rhizomes ≥
leaves > stems, implying low metal mobility in below-ground
plant parts (from roots to rhizomes), and from below- to
above-ground plant parts (to stems and leaves).
T. latifolia is a species tolerant of the high phytotoxic
concentrations of trace elements present in the leachate and
accumulated in the sediment of the Etueffont constructed
wetlands. However, the high amounts of metals found in
the water entering the system, and concentrated in the first
pond's sediments may reach a threshold value for this species,
becoming phytotoxic since plant growth was slightly affected
compared to biomass measured in the fourth and final pond.
Careful management of CWs, with harvesting of aboveground plant parts before senescence at the end of the
growing season (late summer) will therefore be necessary to
prevent unwanted flushing of trace elements back into the
system's ponds. The results presented in this study, from data
collected two years after the maintenance of the constructed
wetland in fall 2009 (i.e., clearing and grading), must be
verified. Further long-term monitoring and studies of the four
interconnected ponds from the Etueffont lagooning system
will be necessary if we are to gain an overview of the seasonal
variations in the metal and metalloid bioaccumulation ability of
T. latifolia in different concentrations.
Acknowledgments
The authors would like to thank the SICTOM (Solid Waste
Management Service) of Etueffont (Territoire de Belfort, France)
for their financial help. The authors also thank Mr. M. Grapin
and Dr. H. Grisey for permitting access to the site.
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four interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039