Metals and metalloid bioconcentrations in the tissues of ... · Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the four interconnected ponds of

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Metals and metalloid bioconcentrations in the tissues ofTypha latifolia grown in the four interconnected ponds of adomestic landfill site

Zohra Ben Salem1, Xavier Laffray1,2,5, Ahmed Al-Ashoor1,3, Habib Ayadi4, Lotfi Aleya1,⁎

1. Bourgogne Franche-Comté University, Chrono-Environnement Laboratory, UMR CNRS 6249, F-25030 Besançon Cedex, France2. Paris Est-Créteil University, IPE team, iEES Paris UMR 7618, F-94010 Créteil Cedex, France3. Thi Qar University, IQ-64001 Al Nasiriyah, Iraq4. Sfax University, LR/UR/05ES05 Biodiversity and Aquatic Ecosystem, BP 1171, CP 3000 Sfax, Tunisia

A R T I C L E I N F O

⁎ Corresponding author. E-mail: lotfi.aleya@u5 The two authors did equal contribution t

http://dx.doi.org/10.1016/j.jes.2015.10.0391001-0742/© 2016 The Research Center for Ec

Please cite this article as: Ben Salem, Z., etfour interconnected ponds of a domestic

A B S T R A C T

Article history:Received 26 June 2015Revised 15 October 2015Accepted 15 October 2015Available online xxxx

The uptake of metals in roots and their transfer to rhizomes and above-ground plant parts(stems, leaves) of cattails (Typha latifolia L.) were studied in leachates from a domesticlandfill site (Etueffont, France) and treated in a natural lagooning system. Plant parts andcorresponding water and sediment samples were taken at the inflow and outflow pointsof the four ponds at the beginning and at the end of the growing season. Concentrations ofAs, Cd, Cr, Cu, Fe, Mn, Ni and Zn in the different compartments were estimated and theirremoval efficiency assessed, reaching more than 90% for Fe, Mn and Ni in spring and fallas well in the water compartment. The above- and below-ground cattail biomass variedfrom 0.21 to 0.85, and 0.34 to 1.24 kg dry weight/m2, respectively, the highest valuesbeing recorded in the fourth pond in spring 2011. The root system was the first site ofaccumulation before the rhizome, stem and leaves. The highest metal concentration wasobserved in roots from cattails growing at the inflow of the system's first pond. The trendin the average trace element concentrations in the cattail plant organs can generallybe expressed as: Fe > Mn > As > Zn > Cr > Cu > Ni > Cd for both spring and fall. WhileT. latifolia removes trace elements efficiently from landfill leachates, attention should alsobe 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.

Keywords:Landfill leachateLagooningTrace elementsTypha latifoliaPhytoremediation

Introduction

Recent years have seen an increase in the application ofconstructed wetland (CW) technology to restore water qual-ity throughout the world, particularly in North and SouthAmerica, Asia and Europe. Presenting great ecological andenvironmental advantages, with economic and social bene-fits as well (Herath, 2004), lagooning systems represent a

niv-fcomte.fr (Lotfi Aleyao this article.

o-Environmental Science

al., Metals andmetalloidlandfill site, J. Environ. S

simple, eco-friendly, affordable and highly efficient biogeo-chemical system to collect, treat and purify waters generatedby various sources including domestic and municipal sew-age, agricultural runoff, storm water and industrial dis-charges, as well as landfill leachate contaminated by traceelements (Vymazal et al., 2010; Grisey and Aleya, 2016a)which may endanger the quality of both surface waters andgroundwater (Council Directive 1999/31/EC).

).

s, Chinese Academy of Sciences. Published by Elsevier B.V.

bioconcentrations in the tissues of Typha latifolia grown in theci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039

http://dx.doi.org/10.1016/j.jes.2015.10.039

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Generated by waste-layer moisture and rainwater infiltra-tions, leachates outflowing from landfill areas are rich innutrients, trace elements and organic compounds which, inturn, depend on waste material type and quantity (Kjeldsenet al., 2002; Bichet et al., 2016). Leachate treatment inconstructed and artificial wetlands (CWs and AWs), beforedischarge into the environment, partly consists of transfer ofpollutants to sediments at the bottom of the ponds via theprocesses of adsorption onto suspended matter and sedimen-tation (Zwolsman et al., 1993). Sedimentation of pollutedparticles resulting in high trace element concentrations in CWsediments are generally considered as a sink (Hart, 1982).Leachate treatment also consists of bioaccumulation in wetlandmacrophytes (Wojciechowska and Waara, 2011). This process,however, is heavily influenced by seasonal variations in macro-phyte growth, by plant tolerance for organic, metallic andnutrient loads, by the concentrations and mobility of elementsin the surrounding water and sediment, and also by bioavailabil-ity (Grisey et al., 2012).

Worldwide studies of emergent macrophytes have dem-onstrated the resistance of these species with respect to waterand sediment contents and especially to high pollution levels.They have a capacity to accumulate and sequester elementsin below-ground (root) plant parts and to a lesser extent inthe above-ground phytomass (Bonanno, 2011). The emergentmacrophyte Typha latifolia (cattail) is one of the widely dis-tributed, tolerant and most productive natural species intemperate aquatic ecosystems (high biomass production andfast growth rate) that is able to grow in harsh conditions(Lyubenova et al., 2013). Thus, this species is commonly usedin wastewater treatment by lagooning for the removal of traceelements (Maddison et al., 2009; Grisey et al., 2012; Kumariand Tripathi, 2015).

Effects of metals and metalloids on components of wet-land treatment areas are of particular concern at the Etueffontlandfill site (Territoire de Belfort, France), a pilot site for traceelement transfer studies in the floating, submerged andemergent species of aquatic plants. Previous studies of thefourth and least polluted pond of the Etueffont CW haveshown that removal through aquatic macrophyte bioaccumu-lation was efficient without a significant effect on cattailgrowth (Grisey et al., 2012; Ben Salem et al., 2014).

The aim of the present study is to give a detailed over-view over a two-season period of metal and metalloidbioconcentration capacities of T. latifolia at the Etueffontsurface flow constructed wetland for landfill leachate treat-ment. Indeed, growing within the site's four interconnectedponds, this macrophyte shows a decreasing gradient ofexposure to trace elements in both water and sediment. Theseasonal growth dynamics of T. latifolia were investigatedand trace element levels (for metals: Cd, Cr, Cu, Fe, Mn, Niand Zn; and for metalloids: As) in the below-ground (rootsand rhizomes) and above-ground plant parts (stems andleaves) were determined, along with concentrations in thecorresponding water and sediment samples. The impact ofseasonal climatic conditions on trace element concentrationsin water and sediment inflow/outflow was studied and thecorresponding level in the plant's above- and below-groundorgans. This enabled us to determine the removal efficiencyof T. latifolia in water quality improvement before discharge

Please cite this article as: Ben Salem, Z., et al., Metals andmetalloidfour interconnected ponds of a domestic landfill site, J. Environ. S

into the environment. Differences in metal and metalloidconcentrations in T. latifolia plant parts and translocationproperties 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 in1976 in order to collect uncompacted ground householdwastes 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 ofaccumulated crushed wastes (15 m thick) was covered by a0.4 m thick layer of artificial soil composed of crushed organicwastes (paper, wood, lawn cuttings, straw, fabrics) (Khattabiet al., 2007). A drainage system was installed for downstreamleachate collection from the two cells and treatment prior towater discharge in a nearby stream, Gros Prés Brook. Theconstructed wetland (CW) is comprised of a series of fourinterconnected lagooning ponds with a total area of 5250 m2.The characteristics of the CW have been previously describedby Ben Salem et al. (2014). The water flowing through theCW was adjusted to 59.4 m3/day during the 2011 monitor-ing periods with a retention time of about 87 days. The fourponds are situated over an underlying 1 m thick layer of claythat has a bed slope of 1%. After maintenance in the fall of 2009(i.e., clearing and grading), the ponds were replanted with newcattail plants (Typha latifolia L.) at a mean density of 1 m−2.

1.2. Water sampling

Three hundred thirty-six water samples were collected in150 mL bottles from each of the four ponds, at (a) threelocations close to the inflow and (b) three locations at theoutflow, every 2 days for 2 weeks, in spring (from 04/18/2011to 05/01/2011) and fall (from 10/17/2011 to 10/30/2011).After collection, samples were stored at 4°C for preservationbefore preparation and analysis. The samples were filteredthrough a 0.45-μm membrane; 25 mL from each sample weretreated with 6 mL of 68% v/v HNO3 before analysis. Fourteensamples of water for background values were collected inGros Prés Brook on the same dates (Fig. 1) and analyzedsimultaneously. Ambient environmental factors at the wet-land study site, namely temperature, pH and electrical con-ductivity (portable multiparameter probe WTW, MultilineP3 PH/LF-SET) were determined in situ for both samplingcampaigns.

1.3. Macrophyte and sediment sampling

Replicate samples were collected individually and processedseparately for both T. latifolia (above- and below-ground plantparts) and sediment from three 1 m2 plots near the inflow andoutflow water collection locations of each of the four ponds:(a) during spring growth (05/01/2011), and (b) after the summergrowth period, in late fall (10/30/2011).



Fig. 1 – Concentrations of As, Cd, Cr and Cu (mg·(kg/DW−1)) in sediment and water collected at inflow and outflow samplinglocations of the four ponds of the lagooning system in spring and fall 2011 (n = 6, mean ± SD). DW: dry weight.

3J O U R N A L O F E N V I R O N M E N T A L S C I E N C E S X X ( 2 0 1 6 ) X X X – X X X

1.3.1. MacrophytesFor the forty-eight samples, each set of roots, rhizomes, stemsand leaves was thoroughly rinsed several times with deion-ized water before oven drying at 80°C to a constant weight(for about 24 hr) (Mishra et al., 2008). The dry samples werereduced to powder in a mortar for analysis. For each plant,a 1-g dry weight sample was digested with 3 mL HNO3 and1 mL H2O2 at 105°C for 3 hr in a microwave digestion system,according to the standard NF EN ISO 15587-2 (2002) beforeanalysis by ICP-OES (Thermofisher Scientific iCAP 6000).

1.3.2. SedimentFor the eight sampling plots, three replicate samples werecollected with a sediment corer (10 cm diameter) at about 10–15 cm depth so as to collect both sludge deposits and a smallportion of the underlying clay. After being wet sieved througha 5.0 mm pore-size polypropylene mesh with reagent gradewater to separate the sediment-size fraction and eliminateplant fragments, the samples were left to settle and the waterwas later decanted. The sediment clay-fractions were frozen at−18°C, according toAnnexeAof the standardNFEN13346. Afterhomogenization using a mortar and pestle, and dry-sievingthrough a 2.0 mm pore-size polypropylene mesh, 1 g of eachsediment samplewas digestedwith 3 mLHNO3 and 9 mLHCl at105°C for 3 hr in amicrowave digestion system. All instrumentswere cleaned before and after each sample with 10% redistilledHNO3 and then rinsed with reagent water.

1.4. Sample analysis

The trace element concentration in water, plant and sedi-ment 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 ofsamples for accuracy and precision. Instrument performanceduring analysis was monitored using an internal standard.For bothmacrophyte and sediment analyses, internal controlstandards were analyzed with each sample and a duplicatewas run for every ten samples. The detection limits withICP-OES were 0.02 mg/L for As, Fe, Mn, Ni and Zn; 0.01 mg/Lfor Cd, Cr and Cu. Data outputs were expressed in mg/L forwater, in mg/kg dry weight for sediment and plant materials.

1.5. Determination of phytoremediation parameters

The biological concentration factor (BCF) was calculated as theratio between trace element concentrations in plant materialand the concentrations in the water to which the macrophyteis exposed (Zayed et al., 1998). This index defines the abilityof T. latifolia to uptake metals and metalloids with respect toconcentrations in the surrounding waters of the lagooningsystem's different ponds.

The translocation properties of T. latifolia are described asratios of trace elements in sediment to those of the above- andbelow-ground plant parts and are expressed in the Enrichmentcoefficient (EC) given in the four following equations (Sasmazand Sasmaz, 2009): ECR = Croot / Csediment; ECRh = Crhizome /Csediment; ECS = Cstem / Csediment; ECL = Cleaf / Csediment.

The translocation factor (TLF) was calculated as elementconcentration ratio of plant leaf to plant roots and is givenin the equation as Cleaf / Croot (Sasmaz and Sasmaz, 2009).The Leaf-Stem Ratio (LSR) was also calculated as the fractionof Cleaf / Cstem.




The biological concentration factor (BCF) as well as en-richment coefficient (EC) and the transfer factor (TLF) werecalculated only for those elements detected in water, sedi-ment and plant organs.

1.6. Statistical analysis

Before conducting any statistical analysis, normality of thedata was checked with a Kolmogorov–Smirnov (KS) test.Statistical differences between inflow and outflow traceelement concentrations in the four ponds were assessedusing a mean comparison test (p < 0.05). Also, bioaccumula-tion and translocation factors determined for the four pondsduring the two sampling periods were statistically analyzedusing amultifactor analysis of variance (ANOVA); differencesamong mean values were evaluated by Tukey's post-testwhen appropriate. In all tests, a significance level of p < 0.05was used for differences in critical values. A linear regres-sion model was used to evaluate the effect of trace elementconcentration in the water solutions on the mean con-centration in T. latifolia plant part biomass. All statisticalanalyses were performed with R statistical analysis system(www.R-project.org).

2. Results

2.1. In-/outflowing water quality

2.1.1. Ambient environmental factorsFrom pond to pond, pH did not vary noticeably during theexperiment (Table 1). Though it increased in spring, with thehighest values recorded at inflow of pond 3 (8.1), no significantseasonal variations were recorded for any pond. For the twosampling periods, water temperature at pond 1 inflow showedgenerally higher values than those found in the remainingthree ponds. However, no significant differences were record-ed for any of the system's ponds (neither at inflow noroutflow). The highest temperature was recorded in spring inpond 1 (11.2°C), but without significant variations betweeninflow and outflow. The water in the lagooning system cooledduring fall, though freezing conditions never occurred duringthe study period; the lowest temperature was recorded atpond 4 outflow (4.6°C).

Electrical conductivity in water varied from spring to fallwith the highest values recorded in spring at pond 1 inflow.Conductivity for both seasons was significantly reduced in

Table 1 –Morphometric and physical characteristics of the four

Pond 1

Temperature (°C) Spring 10.4 ± 0.6Fall 6.4 ± 0.5

pH Spring 7.6 ± 0.1Fall 7.7 ± 0.2

Conductivity (μS) Spring 1792.1 ± 124.2Fall 1687.6 ± 86.4

DO (mg/L) Spring 6.84 ± 3.29Fall 7.68 ± 2.67


ponds 2, 3 and 4 compared to pond 1, with less than 1250 μS/cmat both in- and outflow (Table 1). The mean dissolved oxygen(DO) concentration of water flowing through the system wasnot significantly different between ponds during the 2 samplingperiods. However, high DO values were recorded at pond 1inflow, with the highest DO measured in spring (Table 1).

2.1.2. Metals and metalloids in waterIn-/outflow of the four ponds, and Gros Prés Brook sampleswere analyzed for metal andmetalloid content (As, Cd, Cr, Cu,Fe, Mn, Ni and Zn) (Figs. 1 and 2). Background trace elementconcentrations from samples collected in Gros Prés Brookwere close to or under the detection limits of the ICP-OES(data not shown). Mean concentrations of As, Cd and Cr inwater samples collected at both in- and outflow of the fourponds was generally constant for the two seasons, remainingbelow detection limit values throughout the experiment.Seasonal decreases in trace element content were recordedat 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 andFe were significantly reduced compared to the concentrationsmeasured in ponds 1 to 3 in spring. Mn and Ni levels weresignificantly reduced (p < 0.01) in comparison to the concen-trations measured for spring and fall in ponds 1 and 2 only(Figs. 1 and 2).

For both sampling seasons significant decreases in concen-trations in inflow and outflow waters of the first three pondswere observed for Fe, Mn, Ni and Zn only. Concentrations of Curecorded in in-/outflow waters were significantly reduced forthe two sampling periods in ponds 1 and 2 only. Significanttraceelement concentration removal in the Etueffont treatmentsystem was recorded during both sampling periods (As, Cdand Cr excepted). In-/outflow trace element removal in waterflowing through the entire system varied from −17% to −94% inspring and from −83% to −95% in fall, with a global efficiencyup to 90% for Fe, Mn and Ni (Zn in fall 2011 only). Cu removalefficiency ranged from 83 to 88%.

2.1.3. Metals and metalloids in sedimentsData recorded during the two sampling periods in the fourponds are shown in Figs. 1 and 2. For both spring and fallsignificant decreases in concentrations at inflow and outflowof the first three ponds were observed for As, Cd, Cr, Fe andZn. However, no significant temporal differences were re-corded for Cu or Ni (at inflow or outflow), or Mn (ponds 1 and2 only). In pond 4, in contrast, significant seasonal decreases

interconnected ponds of the Etueffont lagooning system.

Etueffont interconnected ponds

Pond 2 Pond 3 Pond 4

10.3 ± 0.2 9.8 ± 0.2 9.7 ± 0.36.1 ± 0.3 5.7 ± 0.4 5.2 ± 0.47.8 ± 0.1 7.9 ± 0.2 7.6 ± 0.17.8 ± 0.1 7.8 ± 0.1 7.7 ± 0.1

1245.3 ± 38.4 1027.7 ± 23.7 1057.0 ± 13.2952.9 ± 14.9 826.4 ± 16.8 756.8 ± 37.95.23 ± 1.04 5.79 ± 0.84 6.73 ± 1.247.82 ± 0.76 6.38 ± 0.48 5.18 ± 1.32


http://www.R-project.org


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Please cite this article as: Ben Salem, Z., et al., Metals andmetalloid bioconcentrations in the tissues of Typha latifolia grown in thefour interconnected ponds of a domestic landfill site, J. Environ. Sci. (2016), http://dx.doi.org/10.1016/j.jes.2015.10.039


Fig. 3 – Above and below-ground biomass (kg·(DW/m−2)) ofT. latifolia sampled at inflow and outflow of the fourinterconnected ponds in spring and fall 2011(n = 6, mean ± SD).


in metal concentrations at inflow and outflow were observedfor Cd, Cr, Cu, Mn and Zn only. Moreover, no significanttemporal differences were recorded for Fe and Ni (at inflowand outflow) (Fig. 2), or for As (at outflow only) (Fig. 1).

Trace element content in outflow sediment showedgenerally lower values than those found at inflow (Cu andNi except in pond 1). In-/outflow trace element removal insediment 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, whateverthe pond or sampling month. For As, Cr and Fe, concen-trations* were also significantly reduced between inflow andoutflow, in both seasons but only in ponds 1 to 3. Mn levelswere significantly reduced in ponds 2 and 3 only. No sig-nificant removal was recorded for Ni. Cd was significantlyreduced (p < 0.05) compared to the concentrations measuredat inflow for spring and fall in ponds 3 and 4. Significantremoval of metal and metalloid contents was recorded in allponds during both sampling periods (Cu and Ni excepted)with a global efficiency of less than 60% for Cd, Cr, Cu, Mn andNi in spring and fall, but of up to 90% for As in sediment.

2.2. Biological variables

2.2.1. Macrophyte phytomassThe average values of above- and below-ground cattailbiomass harvested during the two study months in the fourponds are shown in Fig. 3. The below-ground plant part (rootsand rhizomes) biomass varied from 0.34 to 1.24 kg DW/m2,the highest value being measured at pond 4 outflow in springand the lowest at pond 1 outflow in fall.

T. latifolia was found to be similar in terms of above-groundbiomass (stems and leaves) in ponds 2, 3 and 4where they grow(Fig. 3) without significant differences between inflow andoutflow sampling points (0.56 ± 0.14 and 0.49 ± 0.16 kg DW/m2

in spring and fall, respectively). The highest shoot biomasswas measured at pond 4 inflow in fall, with 0.85 kg DW/m2.The lowest above-ground macrophyte biomass was recordedin cattails collected at pond 1 inflow for the same samplingperiod (0.21 kg DW/m2).

No significant difference was observed in above- andbelow-ground plant biomass nor in relation to the samplinglocation within ponds 2, 3 and 4, comforting the hypothesisof uniform growing conditions for the plants. However, incomparing the system's first and last ponds, contrastingdata were observed at the beginning and the end of thegrowing season for both above- and below-ground biomass ofT. latifolia. Moreover, cattail total biomass generally decreasedin ponds 1 and 2 in spring and fall, but without significantdifferences between any of the four ponds for spring. Asignificant difference in biomass was observed for emergentmacrophytes collected at pond 1 inflow only.

2.2.2. Metal and metalloid storage in macrophytes andrelationships with sedimentConcentrations measured in T. latifolia during the twosampling periods are shown in Figs. 4 and 5. In most cases,trace element concentrations were significantly higher inroots and rhizomes than in leaves and stems of the T. latifoliagrowing at both inflow and outflow.


2.2.2.1. Below-ground plant parts: Roots. Except for As, B, Cd,Fe and Cu, significant differences in all metal concentrationsbetween the two sampling periods were recorded for roots(p < 0.05), whatever the pond (Figs. 4 and 5). The highest metalconcentrations in T. latifolia were found for Fe and Mn in rootson the inflow side of the first pond in spring with 71,196and 14,939 mg/kg DW, respectively. Whatever the seasonand the sampling location, the lowest metal concentrationswere recorded for Cd in roots with less than 3.19 mg/kg DW(data not shown). In cattail roots, the average metal andmetalloid concentrations in the four ponds can be rankedas follows: Fe > Mn > As > Zn > Cr > Cu > Ni > Cd for the twosampling periods.

2.2.2.2. Below-ground plant parts: Rhizomes. Only Cd and Crdid not vary significantly with season in T. latifolia rhizomes,neither at inflow nor outflow (Figs. 4 and 5) (except for Crat pond 4 inflow). Whatever the pond and the harvestingdate, Cd in T. latifolia rhizome remained below the detectionlimits (BDL). The highest metal concentrations in T. latifoliawere generally found for Fe and Mn in spring in rhizomescollected on the inflow side of pond 1 with 20,203 and 3104 mgper kilogram DW, respectively. Moreover, no significant vari-ations in rhizome were recorded for Cu between the twoperiods at pond 4 outflow. Except for pond 1, the trendin the average metal concentrations in cattail stems was:Fe > Mn > Zn > As > Cu > Ni > Cr for the two sampling periods.

2.2.2.3. Above-ground plant parts: Stems. As, Cd and Crin stems remained below the detection limits (BDL) in theT. latifolia stems harvested from all ponds, regardless ofcollection time (Figs. 4 and 5). Significant differences from



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. latifoliacollected 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 wererecorded for Fe and Zn only (p < 0.05). The highest metal con-centrations in T. latifolia were found for Fe and Mn in stems at

Fig. 5 – Concentrations of Mn, Ni and Zn (mg·(kg/DW−1)) in abovecollected at inflow and outflow sampling locations of the four po(n = 6, mean ± SD).


pond 1 inflow in spring with 1438.7 and 1669.4 mg/kg DW,respectively. The same general trend as in cattail stems wasobserved in leaves with: Mn > Fe > Zn > Cu > Ni for the two

and below-ground biomass (kg·(DW/m−2)) of T. latifoliands of the lagooning system in spring (S) and fall (F) 2011




sampling periods (As, Cd and Cr remaining below thedetection limits).

2.2.2.4. Above-ground plant parts: Leaves. The same patternwas observed among both stems and leaves for As, Cd and Crwith concentrations remaining below the detection limits,regardless of collection time (Figs. 4 and 5). As in roots andrhizomes, trace element concentrations in above-ground plantparts were maximal in spring after plant growth, whereas ageneral decrease occurred in fall with senescence. With theexceptionof the four elements, trace elementuptake byT. latifoliaabove-ground phytomass (stems and leaves) showed similarsignificant seasonal variations to those of below-ground plantparts at inflow and outflow in all four ponds. Significantdifferences either at inflow or outflow in the four lagooningponds between the two sampling periods were recorded for Mnonly (p < 0.05). The highest metal concentrations for Fe and Mnin T. latifoliawere found in stems at pond 1 inflow in spring with571.6 and 4011.8 mg/kg DW, respectively. Except for pond 1, thetrend in the average metal and metalloid concentrations in thecattail rhizomes was as follows: Mn > Fe > Zn > Cu > Ni for thetwo sampling periods (As, Cd and Cr below the detection limits).

2.2.3. Biological concentration factor (BCF) and enrichmentcoefficient (ECR)The ability index of T. latifolia to uptake trace elements fromwater (BCF) for collected plants at inflow and outflow of thefour ponds is summarized in Table 2. Mean values of BCFincreased according to element as follows: Ni < Zn < Cr <Cu < Mn < Fe. The highest BCF values determined were for Feand Mn (in both spring and fall) in pond 4. The elements As

Table 2 – Biological concentration factor (mean ± SD), enrichmefour ponds of the Etueffont lagooning system.

BCF E

Spring 2011 Sprin

Pond 1 Pond 2 Pond 3 Pond 4 Pond 1 Pond 2

As ne ne ne ne 2.73 3.54Cd ne ne ne ne 0.86 0.66Cr 5014 ne ne ne 0.91 0.93Cu 796 1495 2062 3453 0.44 0.32Fe 50,052 70,623 107,273 208,297 0.55 0.73Mn 19,262 36,956 80,529 120,638 3.57 3.49Ni 343 539 1339 2002 1.15 0.9Zn 1074 1230 1284 1337 0.45 0.47

Fall 2011 Fal


As ne ne ne ne 1.33 2.5Cd ne ne ne ne 1.06 0.9Cr ne ne ne ne 0.25 0.3Cu 974 1814 2311 2043 0.46 0.33Fe 41,050 67,997 185,209 317,154 0.53 0.78Mn 11,890 21,662 46,058 62,687 1.46 1.25Ni 149 193 432 782 0.41 0.33Zn 721 823 807 4592 0.23 0.19

BCF: biological concentration factor; EC: enrichment coefficient; ECRh: enECR = Croot / Csediment; ECRh = Crhizome / Csediment.


and Cd were not analyzed in the water, since concentrationswere below the method's detection limit, preventing calcula-tion 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 reportedwere for As in pond 3 (in spring) and Mn in pond 4 (in bothspring and fall). Except for As and Mn, the ECR of T. latifoliawere 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 beingmeasured for Mn in spring (in pond 1). For As and Fe thehighest ECRh values were observed also observed in springonly in both ponds 1 and 2. The rhizome enrichment coef-ficients were from 71% to 98% lower than those found in theroots, with the decrease in elements as follows: Zn < Fe <Cu < Ni < Mn < As < Cr (Cd not evaluated (BDL)). Enrichmentcoefficients for all analyzed elements were below 1.

2.2.3.1. ECS/ECL. The mean enrichment coefficients forstems (ECS) and leaves (ECL) ranged from 0.00 to 0.39 andfrom 0.00 to 0.88, respectively (Table 3). For Mn, the highestECS and ECL values were observed in pond 1 in both springand fall. The mean decrease in ECS and ECL values was asfollows: Fe < Cu < Ni < Zn < Mn and Fe < Zn < Ni < Cu < Mn,respectively. EC was not evaluated for As, Cd and Cr sinceconcentrations remained below detection limits for bothsampling periods. Except for Mn in leaves of T. latifoliacollected at inflow of ponds 1 and 3 (spring), enrichmentcoefficients for all analyzed elements were below 1.

nt coefficient (for roots and rhizomes) of T. latifolia from the

CR ECRh

g 2011 Spring 2011


4.39 3.58 0.16 0.25 0.22 0.160.59 0.64 ne ne ne ne0.92 0.60 0.02 0.02 0.02 0.020.32 0.33 0.09 0.04 0.04 0.030.84 0.72 0.16 0.21 0.17 0.053.79 4.04 0.57 0.29 0.36 0.290.92 0.9 0.17 0.12 0.09 0.060.40 0.39 0.07 0.06 0.06 0.08

l 2011 Fall 2011


2.49 3.78 0.07 0.13 0.15 0.090.60 0.86 ne ne ne ne0.29 0.21 0.02 0.02 ne ne0.31 0.36 0.07 0.04 0.03 0.040.77 0.67 0.05 0.06 0.05 0.021.74 2.18 0.13 0.09 0.12 0.170.30 0.29 0.03 0.02 ne 0.030.19 0.3 0.04 0.04 0.05 0.08

richment coefficients for rhizomes.



Table 3 – Enrichment coefficient (for stems and leaves), leaf/stem ratio and Transfer Factor (leaf/root) of T. latifolia from thefour 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 0.03 0.02 0.02 0.02 0.03 0.02 0.01 0.03 0.78 1.09 0.91 1.54 0.06 0.06 0.04 0.09Fe 0.01 0.01 0.01 0.00 0.01 0.01 0.01 0.00 0.77 0.96 1.02 1.10 0.01 0.01 0.01 0.00Mn 0.35 0.29 0.32 0.38 0.88 0.81 0.87 0.77 2.52 2.85 2.67 2.02 0.25 0.23 0.23 0.19Ni 0.04 0.03 0.03 0.03 0.03 0.02 0.02 0.02 0.86 0.75 0.91 0.93 0.03 0.03 0.03 0.03Zn 0.09 0.08 0.08 0.09 0.02 0.01 0.00 ne 0.29 0.12 0.05 0.04 0.05 0.02 0.01 ne

Fall 2011 Fall 2011 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 Pond 1 Pond 2 Pond 3 Pond 4

Cu 0.02 0.01 0.01 0.02 0.03 0.02 0.03 0.03 1.61 1.51 1.64 1.70 0.06 0.05 0.10 0.09Fe 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.61 1.78 2.77 2.81 0.01 0.00 0.01 0.00Mn 0.39 0.29 0.37 0.33 0.75 0.48 0.59 0.41 1.87 1.63 1.61 1.13 0.51 0.38 0.34 0.19Ni Ne ne Ne Ne 0.02 0.02 0.03 0.03 1.01 ne ne ne 0.06 ne ne neZn 0.05 0.06 0.06 0.07 0.02 0.01 0.00 ne 0.35 0.15 0.09 0.09 0.08 0.05 0.03 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 correlationsbetween 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 twosampling periods the ability of T. latifolia to transfer traceelements from roots to shoots (stems) (TLF) as well as fromstem to leaves (LSR) in the specific conditions that exist in thefour interconnected ponds of the Etueffont lagooning system.The calculated TLF and LSR of T. latifolia in the four pondsare summarized in Table 3. The highest leaf/stem ratio wasobserved for Mn with mean LSR ranging from 2.02 to 2.85 andfrom 1.13 to 1.87 for spring and fall, respectively. High LSRhave also been determined for 2 other metals with meanvalues ranging from 0.78 to 1.7, and 0.77 to 2.81 for Cu andFe, respectively (all sampling dates taken into account) (notevaluated for As, Cd and Cr).

The mean TLF for T. latifolia varied from 0.00 to 0.23 andfrom 0.00 to 0.51 in spring and fall, respectively, (all pondsconsidered), its exclusion capacity found to be: Fe < Ni <Zn < Cu < Mn (Not evaluated for As, Cd and Cr).

3. Discussion

3.1. Metals and metalloids and macrophyte phytomass

In the present study of the four interconnected ponds ofthe Etueffont lagooning system, T. latifolia attained the highestbelow-ground biomass at pond 4 outflow in spring (at pond4 inflow for above-ground biomass). The mean biomass ofaerial parts of T. latifolia, recorded in ponds 2, 3 and 4 (rangingfrom 0.48 ± 0.14 to 0.61 ± 0.12 to kg DW/m2) in both springand fall, were within the same range of above-ground yields


reported for natural stands in the north central United Statesby Pratt et al. (1984) (4.3–14 t DW/ha) and were in accordancewith biomass values measured by Maddison et al. (2009,Estonia). Though above-ground biomass of T. latifolia collectedin the Etueffont CW was generally greater than that reportedby Atkinson et al. (2010) in temperate freshwater marshes insouthwestern Virginia (USA), the biomass of cattail samplesfrom pond 1 at Etueffont remained lower compared to thatrecorded by Atkinson et al. (2010) in freshwater ecosystems.Observations in the cattail population in natural and con-structed wetlands reported in the literature indicate that traceelement concentrations in the sediment in Etueffont's ponds2, 3 and 4 did not significantly affect T. latifolia growth, whilein pond 1 they had a stunting effect. On the contrary, the highconcentrations of metals recorded at pond 1 inflow led to asignificant reduction in macrophyte development (maximumlength of fully expanded leaves, number of leaves, length ofstems, etc.) as well as in the total phytomass of the studiedcattails. Growth reduction along with the increasing traceelement concentrations in both sediment and water arepositively correlated to the reduction of the BCF for Cu, Fe,Mn, Ni and Zn of the macrophytes growing in all four of thesystem's ponds, and also to the ECR reduction of Fe and Mn(the two most concentrated elements in the sediment).

3.2. Water and sediment analyses

3.2.1. Water analysisConcentrations of Cu, Fe and Zn in water passing throughponds 1 to 3 of the Etueffont lagooning system varied notablyduring the two study seasons (p < 0.05). Variations in con-centrations of these five elements in all four interconnectedponds decreased along the water flow path. However, inpond 4 (before discharge into Gros Prés Brook), a significantseasonal inflow/outflow decrease was recorded only for Feand Zn (in spring) and Mn (in fall). For As, Cd and Cr, the




concentrations in the water entering the system remainedbelow the detection limits during the study period. Theobserved concentrations of elements in the water enteringthe Etueffont system were in the same range as in theleachates frommixedmunicipal solid waste landfills reportedby Kjeldsen et al. (2002) in a wide range of studies or thosefound by Justin and Zupančič (2009) from a CW with sixinterconnected ponds designed for landfill leachate pre-treatment (Slovenia). However, data collected at the EtueffontCW inflow were generally higher than (for Cd, Cr, Cu, Mn,Ni, Zn) or similar to (for Fe) observations usually reported fordomestic wastewater or landfill leachate treatment systems(Peverly et al., 1995). Moreover, metal concentrations werehigher in spring than in fall, whatever the pond, corroboratingthe results of Grisey et al. (2012) observed in the fourth pondof the same experimental site. These increases may resultfrom the increased spring rainfall which leads to increasedrainwater infiltrations, waste-layer moisture and lixiviation(Khattabi et al., 2007; Grisey and Aleya, 2016b). The elementconcentrations may also be removed less efficiently fromwater flowing through the system due to a reduced fixationduring winter and early spring due to low or total absence ofbiological activity.

3.2.2. Sediment analysisMetal concentrations in the sediments collected from the fourEtueffont ponds were similar (for Ni) or higher than (for Cd, Cuand Zn) the typical ranges of metal concentrations measuredin 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 andCr, metals and metalloids in the Etueffont sediment generallyexceeded the freshwater sediment quality guidelines deter-mined by MacDonald et al. (2000) in their evaluation ofsediment chemistry concentrations.

Compared to data measured in the horizontal or verticalsubsurface flow of constructed wetlands studied bySamecka-Cymerman et al. (2004), the sediments in the fourEtueffont ponds were generallymore contaminated, showinghigher concentrations of Cd, Cu, Fe, Mn and Zn. Moreover, thepresent study reported very similar (Ni) or higher (Cd, Cu, Mnand Zn) concentrations of elements when compared to thevalues recorded by Sasmaz et al. (2008) in Kehli Stream(Elazig, Turkey).

As for water, trace element concentrations in sedimentsamples collected at Etueffont showed higher values in springthan in fall. As reported by Goulet and Pick (2001), the springpeak in sediment could be the result of increased input, butalso of a lower photosynthesis rate of macrophytes in thesystem impacting element uptake. Moreover, the reductivedissolution/oxidative reprecipitation cycle of redox sensibleelements such as Fe and Mn may affect speciation whichlargely controls element bioavailability of other metals.Thus, increased concentration of Fe or Mn in spring is inducedwhen these elements are dissolved to particulate phasesin metal transformations in suboxic and anoxic conditions(lowmicrobial respiration) (Zaaboub et al., 2014). The decreaseobserved in intermediate redox conditions in fall is caused byreoxygenation and a release of these elements into the waterflowing through the system.


3.3. Root and rhizome metal and metalloid storage from waterand sediments

Analysis of the macrophytes growing at inflow/outflow of thefour ponds indicated that Fe and Mn were the two mostconcentrated elements in below-ground plant parts (roots andrhizomes) of T. latifolia (more effectively in spring than in fall).Though not always similar, depending on the specific wetlandand climatic conditions, the values are in accordance withthose reported by Sasmaz et al. (2008) for Cu, Mn, Ni, and Znfrom T. latifolia in a Turkish stream, but higher values wereobserved for Cd and Mn in the Etueffont system. Furthermore,Cu and Zn concentrations measured in Etueffont T. latifoliabelow-ground organs are similar to those reported in cattailsfrom Estonian wetlands by Maddison et al. (2009), but higherthan those observed by Tanner (1996) in New Zealand or byKlink et al. (2013) in Poland. Moreover, the levels of Cr incattails from the Etueffont ponds were generally similar tovalues reported for the less polluted sites of the MexicanTanque Tenorio artificial wetland (Carranza-Álvarez et al., 2008).However, average concentrations of Fe and Mn at Etueffontwere generally higher than those reported (Carranza-Álvarezet al., 2008; Klink et al., 2013) for cattail roots growing in manyconstructed wetlands.

The roots of macrophytes such as T. latifolia act as filtersin order to avoid the potential toxic effects induced by highelement concentration in above-ground plant tissues. Thus,though toxic elements such as Cd, Cr and Ni (with Cu and Znto a lesser extent) were highly concentrated in the surround-ing sediment, uptake and accumulation of these metals inbelow-ground plants parts were limited with a lower uptakeachieved in rhizomes compared to roots (mean ECR: 0.19 to1.15; mean ECRh: from 0.01 to 0.04). Observations on cattailroots are in accordance with Ahmad et al. (2010) and Klinket al. (2013), who demonstrated the bioaccumulation capacityof these tissue associated with a strong ability to limit root-shoot transfer developed by metal tolerant species (supportedby low ECL and TLFs values below 0.1), most likely due toinefficient metal transport systems (Zhao et al., 2002). Thelimitation of transfer towards and bioaccumulation in rhi-zomes and above-ground plant parts (stems and leaves),characteristic of excluding species (Peverly et al., 1995; Weisand Weis, 2004) is in opposition to facilitated uptake andtranslocation of metals as observed in hyper accumulatorplants. This accumulation in roots by most vascular macro-phytes is strongly related to the low selectivity for metalspresent in the surrounding environment due to the lacunarsystem of large intercellular air spaces of the cortex paren-chyma (Sawidis et al., 1995).

In addition, elements involved in photosynthetic processessuch 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 andMn, respectively) whatever the pond. However, root systemsdo exert a strong selection since scarcely any Fe and Mn weretransferred from root to rhizome, as indicated by low ECRhvalues for most metals (mean ECRh: from 0.02 to 0.16 andfrom 0.09 to 0.57 for Fe and Mn, respectively).

Thus, in accordance with results previously described inthe literature, element concentrations observed in the well-developed root system of most vascular macrophytes appear




to reflect the fact that higher metal concentrations aregenerally to be found in surrounding sediment than is usuallythe case in wetland waters where they remain at low levels(Sawidis et al., 1995). This also supports results described byDeng et al. (2004) and Aksoy et al. (2005) who postulatedthat elements taken up by rooted helophytes and stored inbelow-ground organs were mainly sediment derived. How-ever, the route of exposure (and bioavailability) dependsmainly on water/sediment metal exchange and elementinteraction, which are affected by the environmental charac-teristics of water and sediment (Temperature (°C), OxidationReduction Potential (ORP), pH, water ion content, and salinityconditions) (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 thestem and leaf parts of T. latifolia growing in ponds 1 to 3 werefound to be higher (for Fe, Mn, Zn) or within the same range(for Cu, Cd and Ni) of values given for stems and leaves ofT. latifolia growing in Polish ponds (Klink et al., 2013). Exceptfor Mn, metal concentrations in T. latifolia stems and leaveswere lower than those reported by Sasmaz et al. (2008)(Turkey). Though values of Cd, Cu and Zn similar to thosereported by Maddison et al. (2009) (Estonia) were recorded forleaves from Etueffont, greater concentrations were observedfor Zn in stems (except in fall in pond 4). Concentrationsof these elements during the present study remained belowthe 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-groundorgans from cattails sampled in the Etueffont ponds weregenerally in the same range of values as those found forthe same species collected in the Mexican Tanque Tenorioartificial wetland (Carranza-Álvarez et al., 2008), but repre-sented 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 concentrationsrecorded in the Etueffont ponds exceeded the thresholdvalues defined by Allen (1989) and Markert (1992) (300–500and 30–700 mg/kg, respectively) as toxic for plants, surpassingthe harmful effect limits reported by Pais and Jones (2000).These two elements are directly or indirectly involved aspromoters (or inhibitors, such as Mn in the case of chlorophyllbiosynthesis) in many biological processes including photo-synthesis, respiration, redox enzymatic processes, photo-chemical nitrate and nitrite reduction, N2 fixation, nitrogenmetabolism and carbohydrate utilization (Pais and Jones,2000; Memon et al., 2001; Carranza-Álvarez et al., 2008).

The transfer factor (TLF) generally showed low transport ofelements from roots to shoots (Table 3), not exceeding 1.Uptake and bioaccumulation of Cu, Fe, Ni and Zn in above-ground tissues (both stems and leaves) were very limited (ECSand ECL <0.2), indicating the inefficient translocating actionfrom the root and rhizome system to the aerial plant parts.This relative immobilization of metals in the root system isverified by the determined TLF, which underlines the exclud-ing behavior of the studied macrophyte as a metallophytespecies (Bonanno, 2011; Klink et al., 2013). However, some


elements are less immobilized in below-ground organs asshown by their increased ECS, ECL and TLF values. Thus,though Fe was sequestred in below-ground plant parts, Mnwas more easily transported than other elements and washeavily concentrated in leaves of T. latifolia sampled at inflowas well as at outflow of all four of the interconnected Etueffontponds (mean ECL and TLF: from 0.41 to 0.88 and from 0.19 to0.51, respectively). The same results were observed by Sasmazet al. (2008) with TLF values ranging from 0.39 to 1.18. Theseresults are also in accordance with the observations of Klinket al. (2013) assuming leaves to be the second storage site afterthe root system for Mn.

Thus, the excluding ability of T. latifolia under the con-ditions 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 signif-icant differences in transfer factor were observed betweenponds in spring 2011. For fall 2011, significant variations wereobserved with increasing TLF for Cu, decreasing for Fe and Mnwith the decreasing concentrations of elements in the fourponds.

Lower concentration of metals observed in stems andleaves than in roots may be related to protective mechanismsdeveloped by tolerant plants to cope with metal stressinduced by surrounding water and sediment, and to preventtoxic elements from penetrating into above-ground organsso as to avoid deleterious effects on metabolism and photo-synthesis (Peverly et al., 1995). This sequestration processmay result from the physical absorption of potentially toxicelements at extracellular negatively charged sites in theroot-cell wall of cattails (cell wall-bound fraction) (Mangabeiraet al., 1999). However, metal sequestration of phytotoxicelements as well as the translocation of essential elementsfrom below- to above-ground plant parts may be affected byconflicting and synergetic inter-element processes. Seasonalplant growth dynamics (season-dependent physiology) andseasonal storage and detoxification ability may also greatlyinfluence metal transport between the different plant organs(Mishra et al., 2008). On the other hand, though essentialas oligoelements for plant metabolism and abundantlytranslocated from roots into above-ground tissues for meta-bolic use, elements such as Cu, Fe, Mn and Zn needed asmetabolism cofactors may produce adverse effects if con-centrations exceed threshold limit values in plant tissues.Thus, plants heavily exposed to metals present importantalterations in their photosynthetic processes (Baszynskiet al., 1980; Memon et al., 2001), affecting the photosyntheticelectron transport (Siedliecka and Baszynski, 1993), photo-phosphorylation (Baszynski et al., 1980), carbon fixationcapacity (Bienfait, 1988), carbohydrate metabolism (Borkertet al., 1998) and enzyme activity or protein function (Bonannoand Lo Giudice, 2010).

High concentrations of both essential and toxic elementshave been shown to affect photosynthetic pigment synthesisand degradation (Stiborova et al., 1986) and chloroplastultrastructure (Stoyanova and Chakalova, 1990). Disturbancesin nutrient uptake and sulfate assimilation (Baszynski et al.,1980), water balance (due to alteration of plasma membraneproperties) (Sanità di Toppi and Gabbrielli, 1999), root growthand proliferation (Šottníková et al., 2003) have also been




described in the literature as metal concentrations surpassedcritical values. Thus, most of the Mn (along with otherelements translocated to above-ground plant parts) is proba-bly concentrated in a non-toxic form in the cell walls ofthe epidermis, collenchyma, bundle sheath cells, and in aleaf vacuolar compartment and apoplast, away from meta-bolically active compartments, e.g., cytosol, mitochondria andchloroplast, as reported by Memon et al. (1981).

Defined as a metal tolerance strategy so as to protect aerialplant parts from metal-induced injuries, sequestration pro-cesses 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 macro-phyte bioaccumulation was analyzed in the four interconnect-ed ponds of the Etueffont lagooning system. Trace elementconcentrations inwater and sediments aswell as in above- andbelow-ground plant parts of T. latifolia were examined. Resultsshow that constructed wetland systems can effectively treatlandfill leachates to achieve high quality effluent that canbe discharged into the environment without danger to eithersurface water or groundwater. Concentrations of Fe, Mn, Ni andZn in water were significantly reduced in ponds 1 to 3 for thetwo studied seasons, the maximum reduction being observedfor iron in pond 3 in fall 2011 (−80%).

Concentrations of the studied metals in T. latifolia planttissues generally decreased as follows: roots > rhizomes ≥leaves > stems, implying low metal mobility in below-groundplant parts (from roots to rhizomes), and from below- toabove-ground plant parts (to stems and leaves).

T. latifolia is a species tolerant of the high phytotoxicconcentrations of trace elements present in the leachate andaccumulated in the sediment of the Etueffont constructedwetlands. However, the high amounts of metals found inthe water entering the system, and concentrated in the firstpond's sediments may reach a threshold value for this species,becoming phytotoxic since plant growth was slightly affectedcompared to biomass measured in the fourth and final pond.

Careful management of CWs, with harvesting of above-ground plant parts before senescence at the end of thegrowing season (late summer) will therefore be necessary toprevent unwanted flushing of trace elements back into thesystem's ponds. The results presented in this study, from datacollected two years after the maintenance of the constructedwetland in fall 2009 (i.e., clearing and grading), must beverified. Further long-term monitoring and studies of the fourinterconnected ponds from the Etueffont lagooning systemwill be necessary if we are to gain an overview of the seasonalvariations in themetal andmetalloid bioaccumulation ability ofT. latifolia in different concentrations.

Acknowledgments

The authors would like to thank the SICTOM (Solid WasteManagement Service) of Etueffont (Territoire de Belfort, France)


for their financial help. The authors also thank Mr. M. Grapinand Dr. H. Grisey for permitting access to the site.

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Metals and metalloid bioconcentrations in the tissues of ... · Metals and metalloid bioconcentrations in the tissues of Typha latifolia grown in the four interconnected ponds of