Chemical Engineering Journal 290 (2016) 232242

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Chemical Engineering Journal

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

Review

Accumulation of heavy metals in aboveground biomass of Phragmites

australis in horizontal flow constructed wetlands for wastewater
treatment: A review
Jan Vymazal , Tereza Brezinov
Czech University of Life Sciences Prague, Faculty of Environmental Sciences, Kamyck 129, 165 21 Praha 6, Czech Republic

h i g h l i g h t s

Amount of heavy metals in plant tissue in constructed wetlands is highly variable.

Heavy metals in aboveground plant tissue may represent up to 60% of the inflow load.

Heavy metals in plant tissue may represent a large part of the removed elements.

The highest accumulation in aboveground plant tissues was observed for zinc.

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

Article history: Wastewater treatment in constructed wetlands is a biotechnological process which has been used for
Received 6 October 2015 more than five decades for wastewater treatment. It is generally agreed that plants are important part
Received in revised form 25 December 2015 of the treatment system, however, the direct role of plants is usually restricted to plant uptake of nutri-
Accepted 26 December 2015
ents and heavy metals. The purpose of this study was to evaluate the amount of heavy metals seques-
Available online 25 January 2016
tered in the aboveground biomass of Phragmites australis and thus, available for harvest and removal.
The survey revealed that the amount of heavy metals accumulated in the aboveground plant biomass
Keywords:
(aboveground standing stock) represents often only small fraction of the inflow annual load but in some
Phragmites australis
Biomass
studies, this fraction is quite high, especially for zinc (up to 59%), more rarely for cadmium (55%) and
Heavy metals chromium (38%). The amount of heavy metals sequestered in the plant shoots as a fraction of total
Constructed wetlands removed heavy metal in the constructed wetland is variable with values as high as 71% for cadmium,
Accumulation 55% for chromium or 49% for zinc in some studies. However, there is still a large gap in our knowledge
on heavy metal accumulation in aboveground tissues, namely the conditions that would promote heavy
metal uptake and subsequent translocation to aboveground biomass.
2016 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233
2. Heavy metals concentrations in aboveground biomass of P. australis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234
3. Accumulation of heavy metals in aboveground biomass of P. australis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234
3.1. Accumulation of cadmium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
3.2. Accumulation of lead . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
3.3. Accumulation of nickel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238
3.4. Accumulation of copper . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238
3.5. Accumulation of zinc . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238
3.6. Accumulation of chromium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239

Corresponding author. Tel.: +420 22438 3825.

E-mail address: vymazal@yahoo.com (J. Vymazal).

http://dx.doi.org/10.1016/j.cej.2015.12.108
1385-8947/ 2016 Elsevier B.V. All rights reserved.
 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242 233

4. Overall synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239

5. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

1. Introduction texture sediments and organic matter in the filtration bed and
could be retained by filtration and deposition in the rhizosphere
Wastewater treatment in constructed wetlands (CWs) is a [7]. Heavy metals ae also taken up by roots of macrophytes and
biotechnological process that has been used for more than five dec- could be translocated upwards to the aboveground parts (Fig. 1).
ades [1]. Constructed wetlands are engineered systems that have More details on plant uptake and translocation in Section 3.
been designed and constructed to utilize processes occurring in The presence of macrophytes is one of the most conspicuous
natural wetlands but do so within a more controlled environment. features of wetlands and their presence distinguishes constructed
CWs can be classified according to several criteria, namely wetland wetlands from unplanted soil filters or lagoons. The macrophytes
hydrology free water surface (FWS) and subsurface systems. The growing in HF CWs have several properties in relation to the treat-
subsurface flow systems can be further classified according to the ment process that make them an essential component of the
flow direction (vertical and horizontal) [2]. Horizontal-flow con- design [5]. The plants used in HF CWs designed for wastewater
structed wetlands (HF CWs) are continuously fed with wastewater treatment should therefore (1) be tolerant of high organic and
and therefore the filtration bed is continuously waterlogged and nutrient loadings, (2) have rich belowground organs (i.e., roots
hence anoxic or anaerobic. Vertical-flow constructed wetlands and rhizomes) in order to provide substrate for attached bacteria
(VF CWs) are fed intermittently and each new batch of wastewater and oxygenation (even very limited) of areas adjacent to roots
is brought to the wetland surface only after all the water from the and rhizomes, and (3) have high aboveground biomass for winter
previous batch has percolated. Thus, for some time, the filtration insulation in cold and temperate regions and for nutrient and
bed is empty, oxygen can diffuse there from the atmosphere and heavy metals removal via harvesting [8,9]. The most commonly
therefore, VF CWs are predominantly aerobic. At present, the most used plants are Phragmites australis (Common reed), Phalaris arun-
commonly used CW type is that with horizontal subsurface flow. dinacea (Reed canarygrass), Typha spp. (Cattails) and Scirpus spp.
These systems consist of gravel or rock beds sealed by imperme- (Bulrushes). However, by far the most frequently used species is
able liner and planted with wetland macrophytes. Mechanically P. australis that is also probably the most studied wetland macro-
pretreated wastewater is fed at the inlet and flows through the phyte in natural wetlands [e.g., 1012].
porous media below the surface of the bed in a more or less hori- It is generally agreed that the major functions of plants in HF
zontal path until it reaches the outflow zone, where it is collected CWs is to create conditions suitable for removal of pollutants
and discharged (Fig. 1). During the passage through the filtration [1,9] and the direct role of plants is limited to uptake of nutrients
media, pollution is removed by microbial degradation as well as and heavy metals. There are numerous studies which revealed that
chemical and physical processes in mosaic of aerobic, anoxic and the presence of vegetation has a positive effect on removal of
anaerobic zones [3]. The aerobic zones in horizontal flow CWs organics [1316], ammonia [1619], (phosphorus [20,21] or faecal
are restricted to thin areas adjacent to roots where oxygen leaks coliforms[15,22]. However, there is limited information on effects
to the substrate (so called ROL, radial oxygen loss) [4,5]. of plants on heavy metals removal. In addition, there is a lack of
In HF constructed wetlands, heavy metals are removed/retained information on removal of heavy metals through their accumula-
by both aerobic and anoxic/anaerobic processes through several tion in aboveground biomass in constructed wetlands. Most stud-
mechanisms (Fig. 1). Probably, the most extensive process under ies have focused only on heavy metal concentrations in the
anaerobic conditions is formation of highly insoluble metal sul- aboveground biomass while the amount of heavy metals seques-
fides. Under anoxic conditions, metals can also form carbonates tered in the aboveground biomass, and thus available for harvest-
which are less stable than sulfides [6]. In aerobic conditions that ing, is seldom reported. The purpose of this paper is to review the
may occur in small areas adjacent to roots due to ROL, heavy met- aboveground standing stocks of heavy metals in P. australis grow-
als may be co-precipitated in ferric oxides, hydroxides or oxyhy- ing in HF constructed wetlands for wastewater treatment and to
droxides (Fig. 1). Also, heavy metals may by adsorbed to fine compare the these standing stocks with annual heavy metals loads.

Translocation

Inflow

Co-precipitation with
Fe(OH)3, FeOOH plaque Uptake by roots

Sorption onto M2+ + H2S MS + 2H+

Outflow
sediment particles CO32- + M2+ MCO3
Sulfide, carbonate formation in
anoxic/anaerobic conditions
Filtration

Fig. 1. Layout of a constructed wetland with horizontal subsurface flow and major processes responsible for heavy metals retention.
234 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242
Table 1
Heavy metals concentrations (mg kg1 DM) in the aboveground (total) biomass of Phragmites australis in natural wetlands and constructed wetlands for wastewater treatment.
Constructed wetlands are highlighted in grey color, maximum concentrations in bold. *Values are ranked according to the Zn concentrations.
2. Heavy metals concentrations in aboveground biomass of
P. australis
Heavy metal concentrations in aboveground biomass of
P. australis growing in natural as well as constructed wetlands for
wastewater treatment are shown in Tables 1 and 2 ([2340], [4
143,48,50,52,5456,58,6064,6669]). In Table 1, concentrations
measured in the whole shoot is presented while Table 2 presents
concentrations separated to leaves and stems. It has been shown
that concentrations of heavy metals vary substantially between
stems and leaves with leaf concentrations being often higher [70].
In general, accumulation of heavy metals in macrophytes
depends on the plant uptake capacity and intracellular transporta-
tion in the plant [7173] and involves several steps, such as (a)
mobilization in the rhizosphere, (b) transport of metals across
the plasma membrane of root cells, (c) xylem loading and translo-
cation, and (d) detoxification and sequestration of heavy metals at
the whole plant and cellular levels [71]. The leaf vacuoles are gen-
erally considered to be the main storage sites for heavy metals in
plants [71,74] and sequestration of heavy metals in the vacuole
is also part of the tolerance mechanism [75]. Therefore, heavy
metal concentrations are commonly higher in leaves as compared
to stems with the exception of zinc which may exhibit higher con-
centrations in stems due to the presence of growth hormone indole
acetic acid, which primarily performs its function in stems [23].
The results shown in Tables 1 and 2 indicate that the highest
heavy metals concentrations are often found in natural eutrophic
or polluted wetlands as compared to constructed wetlands treating
municipal sewage or even landfill leachate. The concentrations of
heavy metals may be very high in case of treatment of wastewaters
with excessive concentrations of a particular heavy metal such as
in the case of chromium in tannery wastewaters [59]. However,
the concentration of heavy metals in the biomass itself does not
provide information about the amount of heavy metals accumu-
lated in the biomass. In order to evaluate this amount, it is neces-
sary to take biomass into consideration. Total storage of a
substance or element in a particular compartment is called stand-
ing stock. Standing stocks in the vegetation are commonly com-
puted by multiplying of concentrations in the plant tissue by
biomass per unit area and are expressed as mass per unit area
(usually g m2 or kg ha1) [76].
The results presented in Table 3 reveal that the P. australis
aboveground biomass in HF CWs varies widely between the val-
ues < 1000 g m2 to more than 11,000 g m2 on dry matter basis
with biomass values being commonly between 2000 and
5000 g m2 [77]. The aboveground biomass of P. australis growing
in natural stands also varies greatly within the similar range as
in constructed wetlands [7880] but the most common values of
maximum biomass are lower, between 1000 and 2000 g m2.
Another difference between the Phragmites biomass in natural
and constructed wetlands is its distribution between above- and
belowground parts. While in natural wetlands, the R/S (Root/
Shoot) ratio is nearly always >1, in HFCWs, this ratio is usually
<1 [33,49,77]. For example, Czkov [76] reported an average R/S
ratio of 7.5 with values ranging between 1.5 and 21.9 in European
wetlands. As a consequence, there is usually more aboveground
biomass available for harvesting (and removal of heavy metals)
in constructed as compared to natural wetlands.
3. Accumulation of heavy metals in aboveground biomass of
P. australis
Availability of heavy metals to plants depends on the chemical
speciation of the metal. In aerobic conditions, the availability of
heavy metals in wetlands is usually controlled by the presence of
iron and manganese precipitates which co-precipitate heavy met-
als [8083]. The rhizosphere in horizontal subsurface flow con-
structed wetlands is usually anoxic or anaerobic but aerobic
conditions may occur in the areas adjacent to roots where oxygen
diffuses into the rhizosphere. As a result of ROL, precipitation of
iron hydroxides and oxyhydroxides leads to the formation of so-
called iron plaque [8486] that may act as a barrier to heavy met-
als uptake owing to adsorption and immobilization of metals by
iron plaque [81,87,88]. In anaerobic conditions, heavy metals
mobility is very much controlled by sulphides which are created
through reaction of heavy metals with hydrogen sulphide after
reduction of sulphate [81]. However, oxygen introduced to the rhi-
zosphere from the roots can induce sulphide dissolution [90,91].
Metal remobilization may also result from acidification of the rhi-
zosphere by plant exudates, namely organic acids such as citric and
malic acids [92,93]. Because of the high binding capacity for metal-
lic micronutrients by soil particles, plants have evolved several
 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242 235

Table 2
Heavy metals concentrations (mg kg1 DM) in leaves and stems of Phragmites australis in natural wetlands and constructed wetlands for wastewater treatment. Constructed
wetlands are highlighted in grey color, maximum concentrations in bold. *Values are ranked according to the Zn concentrations.

strategies for increasing their soil bioavailability. These strategies
include the production of metal-chelating compounds such as
mugenic and avenic acids [94]. Once chelated, metal ions may be
transported across the plasma membrane as a metal-
phytometallophore complex via specialized transporters [71].
The metal absorbed is partitioned between the root system and
the shoots. The degree to which roots retain metal, rather than pass
it to the shoots varies greatly with plant species, the metal, and the
concentration supplied [95]. Metal transport to the shoot primarily
takes place through xylem, a mixed vascular tissue, conducting
water and mineral salts taken in by roots throughout the plant
[71,96]. In the xylem sap moving from roots to leaves, citrate,
nicotinamine, histidine and asparagine are the principal ligands
[93,95,97]. By contrast chelation with other ligands, such as phy-
tochelatins or metallothioneins may route metal predominantly
to root sequestration [98].
It has been suggested that the metal speciation in incoming
water, metal fractionation in sediments and the ability of the plant
to transport metals to aboveground parts are the major factors to
influence heavy metal accumulation in aboveground tissues of
macrophytes [46,95]. Phillips et al. [53] reported that concentra-
tions of Cu, Pb and Zn in sediments were in a good correlation with
concentrations of P. australis in roots but in not in stems and leaves.
Yeh et al. [46] observed very low translocation of copper and zinc
to aboveground biomass of P. australis growing in a constructed
wetland treating river water contaminated by confined swine
operations. Therefore, it is not surprising that the amount of heavy
metals accumulated in aboveground biomass of P. australis
236 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242

Table 3 tions could be found in mine waters [101,102]. Under anoxic con-
Aboveground biomass of Phragmites australis in constructed wetlands with horizontal ditions, cadmium forms very insoluble sulphide (CdS, Eq. (1)) and
subsurface flow.
under slightly reduced to oxidized conditions solid carbonate
Locality Leaves Stems Flowers Total Reference (CdCO3, Eq. (2)) is a major control mechanism for Cd solubility
ABG [103].
Hawkesbury, Australia 788 [104]
2
Zevergem, De Pinte, 1140 [45] S2 Cd CdS 1
Belgium
Kolodeje, Czech Republic 271 967 1238 [31] 2
Ferrara, Italy 900 713 1613 [47] CO2
3 Cd CdCO3 2
Shenzhen, China 1633 [105]
Cicenice, Czech Republic 472 1215 1687 [31] Results presented in Table 4 reveal that standing stock of cad-
Ondrejov, Czech 429 1404 1833 [31] mium in aboveground biomass of P. australis is low and varies
Republic between 0.038 and 2.64 mg m2 in HF CWs. Accumulation of cad-
Prato, Italy 2348 [140]
mium in P. australis growing in other types of constructed wetlands
Brehov, Czech Republic 1207 1280 45 2265 [89]
Slavoovice, Czech 1070 1345 75 2490 [57]
and natural wetlands and accumulation in other plants growing in
Republic CWs is also low (Table 4). Elevated accumulation (14.8 mg m2)
Gravesend, UK 3088 [106] was reported in a mesocosm study where P. australis was grown
Mannersdorf, Austria 3100 [107] together with 19 wetland macrophytes [29]. Despite low amount
Kotencice, Czech 1487 2026 147 3660 [77]
of Cd accumulated in the aboveground biomass, this amount may
Republic
Muscle Shoals, Alabama, 4046 [49] constitute a substantial part of the inflow cadmium load (Table 5).
USA Vymazal and Krsa [111] found 54.6% of the inflow cadmium load
San Michele di Ganzaria, 4071 [108] sequestered in the aboveground biomass of P. australis. On the
Italy
other hand, less than 1% of the inflow load accumulated was found
Radotn, Czech Republic 1628 2450 145 4223 [57]
Nezdice, Czech Republic 2301 2668 101 5070 [77]
in P. australis aboveground biomass in a CW treating landfill lea-
Alstonville, Australia 5090 [109] chate [33]. The authors speculated that the low cadmium accumu-
South Africa 6334 [110] lation was affected by Cd adsorption to heavy iron plaque on the
Studnka, Czech 11,280 [77] roots. The amount of cadmium in the P. australis shoots as a frac-
Republic
tion of removed cadmium load varied between 3.95 and 71.1%,
similar amounts for P. arundinacea varied between 22.1 and 37%
(standing stock) does not correspond with the annual inflow load
(Table 5). The results revealed that plant uptake of cadmium and
(Fig. 2). The results presented in Fig. 1 indicate that there is very
subsequent sequestration in aboveground biomass may contribute
low (e.g. zinc, R2 = 0.293) or no correlation between annual heavy
substantially to cadmium removal in constructed wetlands with
metal inflow load and heavy metal standing stock. This is mainly
horizontal subsurface flow.
because the heavy metals entering the filtration bed of HF CWs
become precipitated either as sulphides or co-precipitated with
3.2. Accumulation of lead
iron oxides or oxyhydroxides in the vicinity of plant roots and thus
become unavailable for plants.
Lead concentration in municipal wastewater is usually
<20 lg L1 [99,100,117], higher concentrations could be found in
3.1. Accumulation of cadmium urban and highway stormwater runoff (up to 100 lg L1) and in
mine waters, the Pb concentrations can exceed 1 mg L1 [99]. Lead
Cadmium concentration in municipal wastewater is usually readily forms insoluble sulphides (Eq. (3)), carbonates (Eq. (4)), sul-
very low and does not exceed 1 lg L1 [99,100]. Higher concentra- phates (Eq. (5)) and chlorides (Eq. (6)) [99,118]. It has also been

140 14 12
Zn standing stock (mg m-2)

Cu standing stock (mg m-2)

Ni standing stock (mg m-2)

120 12 10
100 10
8
80 8
6
60 6
40 4
4
20 2 2
0 0 0
0 2000 4000 6000 8000 0 200 400 600 800 1000 0 200 400 600
Inflow load (mg m-2 yr-1) Inflow load (mg m-2 yr-1) Inflow load (mg m-2 yr-1)

0.7 8.0
1.0
Cr standing stock (mg m-2)
Cd standing stock (mg m-2)
Pb standing stock (mg m-2)

0.6 7.0
0.8 6.0
0.5
5.0
0.4 0.6
4.0
0.3 0.4 3.0
0.2 2.0
0.2
0.1 1.0
0 0.0 0.0
0 100 200 300 400 500 0 20 40 60 80 100 0 50 100 150 200
Inflow load (mg m-2 yr-1)
Inflow load (mg m-2 yr-1) Inflow load (mg m-2 yr-1)

Fig. 2. Relationship between annual inflow heavy metals load and heavy metals standing stock in the aboveground biomass of Phragmites australis growing in HF CWs.
 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242 237

Table 4
Accumulation of heavy metals as standing stock (mg m2) in the aboveground biomass of Phragmites australis in constructed wetlands with horizontal subsurface flow. HF CW
horizontal subsurface flow constructed wetland, VF CW = vertical flow constructed wetlands, FWS CW = free water surface constructed wetland. Accumulation values for other
plants, other CW systems and natural stands added for comparison. Modified from Brezinov and Vymazal [115].

Ref. Plant Location Cd Pb Ni Cu Zn Cr

[44] Phragmites australis Belgium 0.038 0.36 0.57 2.9 30 0.57
[33] Phragmites australis USA 0.08 0.14 4.38 25.2
[33] Phragmites australis USA 0.05 0.10 3.11 17.9
[33] Phragmites australis USA 0.04 0.07 2.13 12.2
[47] Phragmites australis Italy 3.93 9.19 90.3
[111] Phragmites australis Czech Republic 2.64 8.1 8.8 2.75 71
[49] Phragmites australis USA 3.55.7 2281
[112] Phragmites australis Czech Republic 0.05 0.38 3.1 7.7 95 7.74
[51] Phragmites australis Belgium 0.06 0.62 0.46 2.8 29.2 1.23
[57] Phragmites australis Czech Republic 2.64 2.64 5.7 5.2 61.9 1.84
[140] Phragmites australis Italy 3.33
[29] 19 wetland plants, FWS CW China 14.8 67.8 195
[39] 19 wetland plants, FWS CW China 40.6 23.3 24.3
[45] Phragmites australis, VF CW Belgium 0.014 0.44 0.91 7.5 90 0.6
[111] Phalaris arundinacea, HF CW Czech Republic 1.66 8.7 35.7 3.64 56.8
[112] Phalaris arundinacea, HF CW Czech Republic 0.15 0.94 1.62 1.13 7.9 0.26
[113] Phalaris arundinacea, HF CW USA 0.11.1 0.53.6 2.021
[114] Typha latifolia, FWS CW Estonia 0.0020.2 0.020.6 0.29.2 1.153.7
[116] Typha domingensis, FWS CW Argentina 26.8 22.6 22.6
[49] Typha sp., HF CW USA 0.81.9 5.212

[44] Phragmites australis natural stand USA 0.051.1 0.44.4 1.649 0.061.1
[23] Phragmites australis, two lakes Denmark <0.08 <0.8 1.01.5 1426
[36] Phragmites australis, eutrophic lake Poland 2.53
[150] Phragmites australis, tidal wetland Belgium 0.0065 0.0064 0.11 0.50 4.08 0.32
[158] Phragmites australis, urban estuary Portugal 0.162 9.8 3.4 18.6 112 5.0

Table 5
Heavy metals sequestered in the aboveground biomass of Phragmites australis in HF CWs as % of annual inflow load. In parentheses, the amount sequestered in the biomass as a
percentage of total removed heavy metal load. Other plants added for comparison.

Ref. Location Cd Pb Ni Cu Zn Cr
[51] Belgium 0.36 (0.54) 0.25 (0.47) 0.26 (0.52) 0.46 (0.50) 0.9 (1.0) 1.3 (2.0)
[44] Belgium 0.5 1.4
[33] USA 0.56 0.0014 15.4 58.9
[33] USA 0.44 0.0013 13.6 52.3
[33] USA 0.28 0.0007 7.5 28.4
[111] Czech Republic 54.6 (71.1) 0.6 (0.63) 8.2 (8.9) 2.7 (3.3) 3.2 (3.5)
[47] Italy 0.46 (1.8) 4.0 (35) 1.6 (6.1)
[112] Czech Republic 1.4 (3.95) 4.8 (6.5) 12.9 (20.9) 10.0 (12.1) 45.3 (48.5) 38.2 (55.4)
[57] Czech Republic 12.4 (24.4) 4.5 (13.1) 5.1 (7.2) 2.0 (8.2) 4.7 (22.3) 3.8 (8.2)
[140] Italy 0.38 (0.96)
[29] China, mixture of 19 plants 12.3 (13.3) 14.1 (14.7) 16.0 (17.0)
[39] China, mixture of 19 plants 8.5 (9.2) 4.9 (5.1) 10.1 (10.9)
[111] Czech Republic HF CW Phalaris arundinacea 16.9 (22.1) 0.32 (0.35) 16.9 (18.4) 3.7 (4.5) 1.3 (1.4)
[112] Czech Republic HF CW Phalaris arundinacea 3.4 (37) 3.3 (11.5) 10.3 (42.7) 3.6 (10.7) 5.4 (10.4) 5.1 (29.6)
[116] Argentina FWS CW Typha domingensis 4.7 (7.7) 3.1 (6.3) 0.73 (0.82)

shown that lead strongly adsorbs to Fe/Mn oxides but is not from natural stands are frequently <1 mg m2 but Kufel [36]
trapped by Fe oxides, but rather is complexed to organic matter reported accumulation of lead in P. australis a eutrophic lake of
either in the rhizosphere solution or on the root surface [119]. 2.53 mg m2. The authors pointed out that there was no relation-
2
ship between lead content in the sediment and in the biomass sug-
S2 Pb PbS 3 gesting that the species-specific physiology rather than the lead
availability regulates the uptake and upward transport. It has been
2
SO2
4 Pb PbSO4 4 shown that lead translocation to shoots is limited and sequestration
occurs mostly in more lignified tissues of rhizomes [120,121].
CO2
2 Vymazal et al. [57] reported the ratio of 3.45 between belowground
3 Pb PbCO3 5
and aboveground lead sequestration in P. australis biomass in a con-
 2 structed wetlands treating municipal sewage. Lesage et al. [51]
2Cl Pb PbCl2 6
reported the amount of lead accumulated in belowground biomass
The lead standing stock in the aboveground biomass of of P. australis being 11 times higher as compared to the amount
P. australis growing in HF CWs treating municipal sewage is low sequestered in the aboveground biomass in a HF CW in Belgium.
and usually <1 mg m2 (Table 4). Higher accumulation was Also, Peverly et al. [33] found 1015 times less lead accumulated
reported by Vymazal and Krsa [111] for both P. australis and P. in shoots as compared to belowground biomass of P. australis in a
arundinacea (8.1 and 8.7 mg m2, respectively). Liu et al. [29] HF CW treating landfill leachate in New York, USA.
observed the accumulation of 67.8 mg m2 in a mesocosms study Results presented in Table 5 indicate that the amount of lead
in China for a mixture of 19 wetland plants. The reported values sequestered in the aboveground biomass of P. australis represents
238 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242
only very small part of the annual inflow lead load in field-scale
constructed wetlands with highest value of 4.8% reported by
Brezinov [112]. In a mesocosm experiment, Liu et al. [29]
observed up to 14.1% of the inflow load being accumulated in the
shoots of P. australis. There is limited information about accumula-
tion of lead in other plants in constructed wetlands; Vymazal and
Krsa [111] and Brezinov [112] reported the values of 0.32% and
3.3%, respectively (Table 5). The results presented in Table 5
revealed that the amount of lead sequestered in the shoots of
P. australis represents 0.4713.1% of the removed annual load. It
means that accumulation in the belowground biomass and reten-
tion of insoluble forms of lead in the filtration beds are the pre-
dominant processes for lead removal in HF CWs.
3.3. Accumulation of nickel
Concentrations of nickel in municipal wastewater are usually
<20 lg L1 [99,100], higher concentrations in the range of 20
50 lg L1 [65,99] could be found in landfill leachate and concentra-
tions of nickel in mine waters may exceed 20 mg L1 [122]. Under
oxic conditions, nickel sorbs to manganese oxides [123] while
under anoxic/anaerobic conditions nickel forms insoluble sul-
phides [124] or carbonates [125] (Eqs. (7) and (8))
S2 Ni
2
NiS
2 droxides [130,131] and could also be retained in iron plaque on
CO2
3 Ni NiCO3 8
Nickel standing stock in shoots of P. australis in HF CWs varies
between 0.46 and 8.8 mg m2 (Table 4). Higher accumulation
(40.6 mg m2) was reported by Liu et al. [39] in a mesocosm exper-
iment with a mixture of 19 plants and by Vymazal and Krsa [111]
for P. arundinacea (35.7 mg m2). Results shown in Table 5 reveal
that the amount of nickel sequestered in the P. australis shoots rep-
resents 0.2612.9% of the annual inflow load representing 0.52
20.9% of the annual nickel removal. For P. arundinacea, Brezinov
[112] that nickel accumulated in shoots represented 10.3% of the
annual inflow load and 42.7% of the removed nickel amount. In free
water surface CW, Di Luca et al. [116] reported respective values of
4.7% and 7.7% for shoots of Typha domingensis.
3.4. Accumulation of copper
Concentration of copper in municipal sewage varies often
between 10 and 50 lg L1 [99,100,117]. Similar concentrations
could be found in landfill leachate and in urban stormwater runoff
[99] while in mine waters, copper concentration may exceed 5 mg
L1 [122]. Under anoxic conditions, copper forms very insoluble
cuprous (Eq. (9)) and cupric (Eq. (10)) sulphides [124,126] and
hydroxides (Eq. (11)) and carbonates (Eq. (12)), which are of less
importance in the presence of sulphides [127]. Copper also forms
strong complexes with organic matter and can also be bound to
Fe/Mn oxides under oxic conditions [128].
S2 2Cu Cu2 S 9 often higher in the aboveground biomass of wetlands plants. For
S2 Cu2 CuS 10
Cu2 2OH CuOH2 11
CO2
3 Cu
2
CuCO3 12
The copper standing stock in aboveground biomass of
P. australis in HF CWs varied in a very narrow range between
2.13 and 9.19 mg m2 in ten studies from Belgium, Czech Republic,
Italy and USA (Table 4). Higher standing stock in the shoots in a HF
CW (23.3 mg m2) was observed by Liu et al. [39] in a mesocosms
experiment planted with P. australis and 18 other macrophytes.
Accumulation in P. australis shoots in a VF CW (7.5 mg m2),
P. arundinacea in three HF CWs (0.53.64 mg m2) and Typha sp.
in a HF CW (0.81.9 mg m2) were similar to values for P. australis
in HF CWs (Table 4). Higher value of accumulation was reported by
Di Luca et al. [116] for T. domingensis growing in FWS CW in Argen-
tina. In natural wetlands, copper accumulation in P. australis shoots
(0.44.4 mg m2) was comparable to that found in HF CWs
(Table 4).
The copper aboveground standing stock in P. australis growing in
full-scale HF CWs represented 0.4615.4% of the annual inflow load
(Table 5). Available data show that the accumulation of copper in
the shoots of P. australis was responsible for 0.535% of the removed
annual copper load. Results from two HF CWs in the Czech Republic
revealed that 3.63.7% of the annual copper load was accumulated
in the aboveground biomass of P. arundinacea which represented
4.5 and 10.7% of removed copper load.
3.5. Accumulation of zinc
Concentrations of zinc in municipal wastewater, stormwater
runoff and landfill leachate usually vary between 50 and
200 lg L1 [99,100,129], while zinc concentrations in mine drai-
7 nage may exceed 5 mg L1 [99,101]. Under aerobic conditions, zinc
is often associated with Fe and Mn oxides, hydroxides and oxyhy-
plant root surface [132]. Under anoxic conditions, zinc forms very
insoluble sulphides [128,133,134] Eq. (13) and carbonates [131]
Eq. (14).
S2 Zn2 ZnS 13
CO2
3 Zn
2
ZnCO3 14
Results presented in Table 4 indicate that the amount of zinc
sequestered in the aboveground biomass of P. australis in full-
scale HF CWs varies between 12.2 and 95 mg m2 with the average
value of 48.7 mg m2 from eleven studies. Similar values were
obtained for P. australis growing in a VF CW and other plants used
in HF and FWS CWs (Table 4). The limited data available for zinc
accumulation in natural wetlands revealed that the values are in
the range of 1.649 mg m2. Higher value of 195 mg m2 was
recorded by Liu et al. [29] for a mixture of 19 wetland plants in a
mesocosms experiment. Results presented in Table 5 demonstrate
that the zinc aboveground standing stock in P. australis represents
0.945.3% of the total annual inflow load. As compared to P. arun-
dinacea or T. domingensis, the range is much wider (Table 5). Also,
the zinc standing stock in P. australis shoots as percentage of over-
all removed zinc varies widely between 1.0 and 48.5%. Unfortu-
nately, the study Peverly et al. [33] where the amount of zinc
sequestered in the aboveground biomass formed high portion of
the inflow does not indicate the total removal of zinc.
The accumulation of zinc, contrary to most heavy metals, is
P. australis growing in a HF CWs, Vymazal et al. [57] found the ratio
between aboveground and belowground accumulation 1.33, Pev-
erly et al. [33] 1.311.35, Galletti et al. [47] 1.93 and Liu et al.
[29] found aboveground/belowground accumulation ratio of 2.16
for 19 wetland plants in a mesocosm experiment. Zinc plays very
important role in plant metabolism by influencing activities of
hydrogenase and carbonic anhydrase, stabilization of ribosomal
fractions and synthesis of cytochrome. Plant enzymes activated
by zinc are involved in carbohydrate metabolism, maintenance of
the integrity of cellular membranes, protein synthesis, production
and regulation of essential growth hormone auxin synthesis and
pollen formation [135]. Zinc is also required for synthesis of tryp-
 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242
tophan which is a precursor of indole-3-acetic acid (IAA hormone)
[136] which primarily performs its function in stems [23]. Because
of these functions, zinc is often found rather in the aboveground
than belowground biomass of wetland plants.
3.6. Accumulation of chromium
Chromium concentrations in municipal wastewater are usually
found in the range of 110 lg L1 [99,100], in industrial wastewa-
ters the chromium concentrations may exceed 100 lg L1 [99],
tannery wastewaters Cr concentration may amount up to
50 mg L1 [137]. Contrary to most heavy metals, chromium under-
goes a change in oxidation state due to soil oxidationreduction
conditions [138]. Under aerobic conditions, chromium typically
sorbs to Fe, and especially to Mn, oxides [128]. Under anoxic con-
ditions, tends to associate with organic matter as chromium is not
readily incorporated into sulphides [139].
There is substantially less information about chromium stand-
ing stock in aboveground biomass of P. australis growing in HF
CWs (Table 4). The values range between 0.57 and 7.74 mg m2.
Higher values of 24.3 mg m2 and 22.6 mg m2 were reported by
Liu et al. [39] for a mixture of 19 plants in China and by Di Luca
et al. [116] for T. domingensis in a FWS CW in Argentina, respec-
tively. Chromium accumulation in the shoots of P. australis in a nat-
ural stand in New York, USA, varied between 0.06 and 1.1 mg m2
(Table 4). Results presented in Table 5 indicate that the amount of
chromium sequestered in the shoots of P. australis as compared to
annual inflow load is highly variable (1.338.2%). Also, the accu-
mulation in shoots as compared to retained amount of chromium
in the wetland is variable (0.8255.4%).
4. Overall synthesis
Wastewater treatment in constructed wetlands is a biotechno-
logical process which has been used for more than five decades for
wastewater treatment. It is generally agreed that plants are impor-
tant part of the treatment system, however, the direct role of
plants is usually restricted to plant uptake of nutrients and heavy
metals. There is considerable amount of studies aimed at evalua-
tion of nutrient removal via plant harvesting but there is limited
information about accumulation of heavy metals in the above-
ground biomass of plants and, thus, available for harvesting and
removal. Most studies evaluate only concentrations in the plant
tissues but this value itself does not provide information about
the accumulation of heavy metals. Heavy metals concentrations
in wetland plants are commonly substantially higher in roots than
leaves and stems [141146]. This may lead to a conclusion that
accumulation of heavy metals is higher in belowground biomass.
This is often true, but it is not possible to take it for granted and
in the situation when belowground biomass is much lower than
aboveground biomass, the accumulation could be higher above-
ground [147]. In constructed wetlands with horizontal subsurface
flow, belowground to aboveground biomass ratio for P. australis
is commonly <1.0 and occasionally <0.5 [148]. In order to obtain
proper accumulation values, it is necessary to include biomass val-
ues into consideration. Unfortunately, there is a lack of this infor-
mation on aboveground biomass in constructed wetlands. The
most probable reason is that biomass harvesting and processing
is time and labour consuming and very often underrated and not
considered scientific.
Guittonny-Philippe et al. [149] in their review concluded that
many wetland plants act as excluders, i.e. plants that restrict metal
transport to aboveground parts in order to keep shoot concentra-
tions as low as possible. The restricted upward transport of heavy
metals limits the potential toxic effect for plants, however, low
239
concentrations may not mean low accumulation. Van Oosten and
Maggio [151] pointed out that naturally-accumulating plants could
be suitable candidates for phytoremediation but these plants usu-
ally produce low annual biomass and, therefore the amount of
heavy metals sequestered in the aboveground biomass is low. For
this reason plants with high aboveground biomass are better can-
didates for phytoremediation because high biomass compensates
low concentrations of heavy metals in plant tissues [152].
Very important factor in heavy metals accumulation in above-
ground biomass of wetland plants is standing stock seasonality.
In temperate and cold climates, the seasonality of nutrient stand-
ing stock is very much predictable. The maximum standing stock
usually occurs at the time of maximum biomass and then
decreases towards the end of growing season [e.g. 153,154]. On
the other hand, the standing stock seasonality for heavy metals
in wetland plants varies among metals and there is no uniform
pattern [148,153,115,155]. Brezinov and Vymazal [115] found
that maximum standing stock in aboveground biomass of
P. arundinacea occurred in July for cadmium and in June for lead
while maximum accumulation of chromium occurred in Septem-
ber and was stable until January. On the other hand, maximum
nickel standing stock occurred in May and then it steadily
decreased. The authors concluded that various heavy metals follow
different seasonal pattern and therefore, it is not possible to find
optimum time for harvest during the year in order to obtain max-
imum removal of all heavy metals at the same time.
Guittonny-Philippe et al. [149] also pointed out that there still
lack of information about the possibility of repeated plant harvest-
ing and general vegetation management. It has been shown that
repeated harvest of P. arundinacea during the growing season
may increase the amount of removable heavy metals (e.g., Zn or
Cd) but for some heavy metals higher amount was removal with
only one harvest at the peak biomass (e.g., Pb or Hg) [156] The rea-
son for phenomenon is that plants translocate toxic metals to the
aboveground tissues which will senesce as detoxifying mechanism
[157].
In general, there is insufficient number of data on the amount of
heavy metals in aboveground biomass of P. australis and other
plants growing in constructed wetlands with horizontal subsurface
flow. In addition, there is little known about the management
strategies including time and number of harvesting for various
macrophytes.
5. Conclusions
The results of the survey revealed that the accumulation of
heavy metals in the plant shoots is frequently low but highly vari-
able. There is no relationship between the amount of heavy metals
entering the constructed wetland and accumulation in the above-
ground biomass. This could be explained by the fact that heavy
metals are often precipitated in the anoxic/anaerobic filtration
bed and become unavailable for plant uptake.
The amount of heavy metals accumulated in the aboveground
biomass of P. australis (aboveground standing stock) represents
often only small fraction of the inflow annual load but in some
studies, this fraction was quite high, especially for zinc (upto
59%), more rarely for cadmium (55%) and chromium (38%). The
amount of heavy metals sequestered in the plant shoots as a frac-
tion of total removed heavy metal in the constructed wetland is
also variable with values as high as 71% for cadmium, 55% for chro-
mium or 49% for zinc in some studies. However, there have been no
attempts to explain the variability in heavy metal accumulation or
to determine the optimum conditions for heavy metal uptake by
plants in constructed wetlands so far. The survey revealed that
there is a wide gap in our knowledge on heavy metal accumulation
240 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242

in aboveground plant biomass available for harvest and thus, [26] I. Zuidervaart, Heavy Metals in Constructed Wetlands, Academy of Sciences of
the Czech Republic, Botanical Institute, Trebon, Czech Republic, 1996.
removal in constructed treatment wetlands with horizontal sub-
[27] F. Duman, M. Cicek, G. Sezen, Seasonal changes of metal accumulation and
surface flow. distribution in common club rush (Schoenoplectus lacustris) and common reed
(Phragmites australis), Ecotoxicology 16 (2007) 457463.
[28] K. Obolewski, E. Skorbilowicz, M. Skorbilowicz, K. Glinska-Lewczuk, A.M.
Acknowledgement Astel, A. Strzelczak, The effect of metals accumulated in reed (Phragmites
australis) on the structure of periphyton, Ecotoxicol. Environ. Safety 74 (2011)
558568.
The study was supported by Grant No. 20134250 accumulation [29] J. Liu, Y. Dong, H. Xu, D. Wang, J. Xu, Accumulation of Cd, Pb and Zn by 19
of heavy metals in vegetation of constructed and natural wetlands wetland plant species in constructed wetland, J. Hazard. Mater. 147 (2007)
947953.
from the Faculty of Environmental Sciences of the Czech University
[30] M. Zhang, L. Cui, L. Sheng, Y. Wang, Distribution and enrichment of heavy
of Life Science Prague. metals among sediments, water body and plants in Hengshuihu Wetland of
Northern China, Ecol. Eng. 35 (2009) 563569.
[31] J. Vymazal, J. Duek, J. Kvet, Nutrient uptake and storage by plants in
References constructed wetlands with horizontal sub-surface flow: a comparative study,
in: J. Vymazal (Ed.), Nutrient Cycling and Retention in Natural and
Constructed Wetlands, Backhuys Publishers, Leiden, the Netherlands, 1999,
[1] J. Vymazal, Emergent plants used in free water surface constructed wetlands:
pp. 85100.
a review, Ecol. Eng. 61P (2013) 582592.
[32] M.J. Surface, J.H. Peverly, T.S. Steenhuis, W.E. Sanford, Effect of season,
[2] J. Vymazal, Constructed wetlands for wastewater treatment, Water 2 (2010)
substrate composition, and plant growth on landfill leachate treatment in a
530549.
constructed wetland, in: G.A. Moshiri (Ed.), Constructed Wetlands for Water
[3] P.F. Cooper, G.D. Job, M.B. Green, R.B.E. Shutes, Reed Beds and Constructed
Quality Improvement, Lewis Publishers, Boca Raton, Florida, USA, 1993, pp.
Wetlands for Wastewater Treatment, WRC Publications, Medmenham, UK,
461472.
1996.
[33] J.H. Peverly, J.M. Surface, T. Wang, Growth and trace metal absorption by
[4] H. Brix, Gas exchange through the soilatmosphere interface and through
Phragmites australis in wetlands constructed for landfill leachate treatment,
dead culms of Phragmites australis in a constructed wetland receiving
Ecol. Eng. 5 (1995) 2135.
domestic sewage, Water Res. 24 (1990) 259266.
[34] G.F. Estabrook, D.W. Burk, D.R. Inman, P.B. Kaufman, J.R. Wells, J.D. Jones, N.
[5] H. Brix, Do macrophytes play a role in constructed treatment wetlands?, Wat
Ghosheh, Comparison of heavy metals in aquatic plants on Charity Island,
Sci. Tech. 35 (1997) 1117.
Saginaw Bay, Lake Huron, U.S.A., with plants along the shoreline of Saginaw
[6] A.S. Sheoran, V. Sheoran, Heavy metal removal mechanism of acid mine
Bay, Am. J. Bot. 72 (1985) 209216.
drainage in wetlands a critical review, Minerals Eng. 19 (2006) 105116.
[35] K. Drbal, J. Pokorny, J. vehla, J. Bastl, L. Pechar, Cycling of heavy metals in
[7] L. Marchand, M. Mench, D.L. Jacob, M.L. Otte, Metal and metalloid removal in
ponds, in: Proc. Conf. Restoration, Maintenance and Construction of Ponds,
constructed wetlands, with emphasis on the importance of plants and
Hradec Krlov, Czech Republic, 1995, pp. 105110 (in Czech).
standardized measurements: a review, Environ. Pollut. 158 (2010) 3447
[36] I. Kufel, Lead and molybdenum in reed and cattailopen versus closed type of
3461.
metal cycling, Aquat. Bot. 40 (1991) 275288.
[8] J. Brisson, F. Chazarenc, Maximizing pollutant removal in constructed
[37] S.N. Groudev, K. Komnitsas, I.I. Spasova, I. Paspaliaris, Treatment of acid mine
wetlands: should we pay more attention to macrophyte species selection?,
drainage by a natural wetland, in: K.W. Nehring, S.E. Brauning (Eds.),
Sci Total Environ. 407 (2009) 19231930.
Wetland and Remediation II, Battelle Press, Columbus, Ohio, USA, 2002, pp.
[9] J. Vymazal, Plants used in constructed wetlands with horizontal subsurface
133139.
flow: a review, Hydrobiologia 674 (2011) 133156.
[38] L.N.L. Scholes, R.B.E. Shutes, D.M. Revitt, D. Purchase, M. Forshaw, The
[10] S. Bjrk, Ecological investigations of Phragmites communis, studies in theoretic
removal of urban pollutants by constructed wetlands during wet weather,
and applied limnology, Folia Limnol. Scand. 14 (1967) 1248.
Wat. Sci. Tech. 40 (1999) 333340.
[11] A.I. Erlonger, Structure, growth dynamics and biomass of reed (Phragmites
[39] J.G. Liu, G.H. Li, W.C. Shao, J.K. Xu, D.K. Wang, Variations in uptake and
australis) a review, Flora 204 (2009) 331346.
translocation of copper, chromium and nickel among nineteen wetland plant
[12] S.M. Haslam, Phragmites communis Trin.: biological flora of the British Isles,
species, Pedosphere 20 (2010) 96103.
no. 128, J. Ecol. 60 (1972) 585610.
[40] S. Khan, I. Ahmad, M.T. Shah, S. Rehman, A. Khaliq, Use of constructed
[13] C.C. Tanner, J.S. Clayton, M.P. Upsdell, Effect of loading rate and planting on
wetland for the removal of heavy metals from industrial wastewater, J.
treatment of dairy farm wastewaters I. Removal of oxygen demand,
Environ. Manage. 90 (2009) 34513457.
suspended solids and faecal coliforms, Water Res. 29 (1955) 1726.
[41] G. Du Laing, A.M.K. Van de Moortel, W. Moors, P. De Grauwe, E. Meers, F.M.G.
[14] M.E. Kaseva, Performance of a sub-surface flow constructed wetland in
Tack, M.G. Verloo, Factors affecting metal concentrations in reed plants
polishing pre-treated wastewater a tropical case study, Water Res. 38
(Phragmites australis) of intertidal marshes in the Scheldt estuary, Ecol. Eng.
(2004) 681687.
35 (2009) 310318.
[15] S. Dallas, G. Ho, Subsurface flow reedbeds using alternative media for the
[42] P.J. Hocking, Seasonal dynamics of production, and nutrient accumulation
treatment of domestic greywater in Monteverde, Costa Rica, Central America,
and cycling by Phragmites australis (Cav.) Trin ex Steudel in a nutrient-rich
Wat. Sci. Technol. 51 (2005) 119128.
swamp in inland Australia. I. Whole plants, Austr. J. Mar. Freshwat. Res. 40
[16] M.P. Ciria, M.L. Solano, P. Soriano, Role of macrophyte Typha latifolia in a
(1989) 421444.
constructed wetland for wastewater treatment and assessment of its
[43] P.J. Hocking, Seasonal dynamics of production, and nutrient accumulation
potential as a biomass fuel, Biosyst. Eng. 92 (2005) 535544.
and cycling by Phragmites australis (Cav.) Trin ex Steudel in a nutrient-rich
[17] R.M. Gersberg, B.V. Elkins, S.R. Lyon, C.R. Goldman, Role of aquatic plants in
swamp in inland Australia. I. Individual shoots, Austr. J. Mar. Freshwat. Res.
wastewater treatment by artificial wetlands, Water Res. 20 (1986) 363368.
40 (1989) 445464.
[18] S. Naylor, J. Brisson, M.A. Labelle, A. Drizo, Y. Comeau, Treatment of
[44] L. Windham, J.S. Weis, P. Weis, Uptake and distribution of metals in two
freshwater fish farm effluent using constructed wetlands: the role of plants
dominant salt marsh macrophytes, Spartina alterniflora (cordgrass)
and substrate, Wat. Sci. Tech. 48 (2003) 215222.
and Phragmites australis (common reed), Estuar. Coast. Shelf Sci. 56 (2003)
[19] S.E. Mbuligwe, Comparative effectiveness of engineered wetland systems in
6372.
the treatment of anaerobically pre-treated domestic wastewater, Ecol. Eng.
[45] E. Lesage, D.P.L. Rousseau, E. Meers, A.M.K. Van de Moortel, G. Du Laing, F.M.
23 (2004) 269284.
G. Tack, N. De Pauw, M.G. Verloo, Accumulation of metals in the sediment and
[20] J. Coleman, L. Hench, K. Garbutt, A. Sextone, G. Bissonnette, J. Skousen,
reed biomass of a combined constructed wetland treating domestic
Treatment of domestic wastewater by three plant species in constructed
wastewater, Water Air Soil Pollut. 183 (2007) 253264.
wetlands, Water Air Soil Pollut. 128 (2001) 283295.
[46] T.Y. Yeh, C.C. Chou, C.T. Pan, Heavy metal removal within pilot-scale
[21] L.H. Fraser, S.M. Carty, D. Steer, A test of four plant species to reduce total
constructed wetland receiving river water contaminated by confined swine
nitrogen and total phosphorus from soil leachate in subsurface wetland
operations, Desalination 249 (2009) 368373.
microcosms, Bioresour. Technol. 94 (2004) 185192.
[47] A. Galletti, P. Verlicchi, E. Ranieri, Removal and accumulation of Cu, Ni and Zn
[22] F. Soto, M. Garcia, E. de Luis, E. Becares, Role of Scirpus lacustris in bacterial
in horizontal subsurface flow constructed wetlands: contribution of
and nutrient removal from wastewater, Wat. Sci. Tech. 40 (1999) 241247.
vegetation and filling medium, Sci. Total Environ. 408 (2010) 50975105.
[23] H.-H. Schierup, V.J. Larsen, Macrophyte cycling of zinc, copper, lead and
[48] V.J. Larsen, The significance of atmospheric deposition of heavy metals in four
cadmium in the littoral zone of a polluted and non-polluted lake. I.
Danish lakes, Sci. Total Environ. 30 (1983) 11127.
Availability, uptake, and translocation of heavy metals in Phragmites
[49] L.L. Behrends, E. Bailey, M.J. Bulls, H.S. Coonrod, F.J. Sikora, Seasonal trends in
australis (Cav.) Trin, Aquat. Bot. 11 (1981) 197210.
growth and biomass accumulation of selected nutrients and metals in six
[24] H. Deng, Z.H. Ye, M.H. Wong, Accumulation of lead, zinc, copper and cadmium
species of emergent aquatic macrophytes. in: Proc. 4th Int. Conf Wetland
by 12 wetland plant species thriving in metal-contaminated sites in China,
Systems for Water Pollution Control, Guangzhou, China: ICWS94 Secretariat,
Environ. Pollut. 132 (2004) 2940.
1994, pp. 274289.
[25] A.S. Mungur, R.E. Shutes, D.M. Revitt, M.A. House. An assessment of metal
[50] A. Aksoy, D. Demirezen, D. Duman, Bioaccumulation, detection and analyses
removal from highway runoff by a natural wetland. In: Proc. 4th International
of heavy metal pollution in Sultan Marsh and its environment, Water Air Soil
Conference Wetland Systems for Water Pollution Control. ICWS94
Pollut. 164 (2005) 241255.
Secretariat, Guangzhou, China, 1994, pp. 669676.
 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242
[51] E. Lesage, D.P.L. Rousseau, E. Meers, F.M.G. Tack, N.D. Pauw, Accumulation of
metals in a horizontal subsurface flow constructed wetland treating domestic
wastewater in Flanders, Belgium, Sci. Total Environ. 380 (2007) 102115.
[52] G. Du Laing, G. Van Ryckegem, F.M.G. Tack, M.G. Verloo, Metal accumulation
in intertidal litter through decomposing leaf blades, sheaths and stems of
Phragmites australis, Chemosphere 63 (2006) 18151823.
[53] D.P. Phillips, L.R.D. Human, J.B. Adams, Wetland plants as indicators of heavy
metal contamination, Mar. Pollut. Bull. 92 (2015) 227232.
[54] M.A. Fawzy, N. El-sayed Badr, A. El-Khatib, A. Abo El-Kassem, Heavy metal
biomonitoring and phytoremediation potentialities of aquatic macrophytes
in River Nile, Environ. Monitor. Assess. 184 (2012) 17531771.
[55] R. Baudo, E. Canzian, G. Galanti, P. Guilizzoni, G. Rapetti, Relationship
between heavy metals and aquatic organisms in Lake Mezzola hydrographic
system (Northern Italy), 6. Metal concentrations in two species emergent of
macrophytes, Mem. Inst. Ital. Idrobiol. 43 (1985) 161180.
[56] T. Suzuki, K. Mariyama, Y. Kurihara, Distribution of heavy metals in a reed
marsh on a riverbank in Japan, Aquat. Bot. 35 (1989) 1212127.
[57] J. Vymazal, L. Krpfelov, J. vehla, V. Chrastny, J. tchov, Trace elements in [86]
Phragmites australis growing in constructed wetlands for treatment of
municipal wastewater, Ecol. Eng. 35 (2009) 303309.
[58] G. Bonanno, R. Lo Giudice, Heavy metal bioaccumulation by the organs of
Phragmites australis (common reed) and their potential use as contamination
indicators, Ecol. Ind. 10 (2010) 639645.
[59] C.S.C. Calheiros, A.O.S.S. Rangel, P.M.L. Castro, The effects of tannery
wastewater on the development of different plant species and chromium
accumulation in Phragmites australis, Arch. Environ. Contam. Toxicol. 55
(2008) 404414.
[60] C. Mant, S. Costa, J. Williams, E. Tambourgi, Phytoremediation of chromium
by model constructed wetland, Bioresour. Technol. 97 (2006) 17671772.
[61] H. Obarska-Pempkowiak, Removal and retention of selected heavy metals in
components of a hybrid wetland system, in: . Mander, P. Jenssen (Eds.),
Constructed Wetlands for Wastewater treatment in Cold Climates, WIT Press,
Southampton, UK, 2003, pp. 299309.
[62] A. Szymanowska, A. Samecka-Cymerman, A.J. Kempers, Heavy metals in three
lakes in west Poland, Ecotoxicol. Environ. Safety 43 (1999) 2129.
[63] A. Samecka-Cymerman, D. Stepien, A.J. Kempers, Efficiency in removing
pollutants by constructed wetland purification systems in Poland, Part A, J.
Toxicol. Environ. Health 67 (2004) 265275.
[64] A. Samecka-Cymerman, A.J. Kempers, Concentrations of heavy metals and
plant nutrients in water, sediments and aquatic macrophytes of
anthropogenic lakes (former open cut brown coal mines) differing in stage
of acidification, Sci. Total Environ. 281 (2001) 8798.
[65] D.A.V. Eckhardt, J.M. Surface, J.H. Peverly, A constructed wetland system for
treatment of landfill leachate, Monroe County, New York, in: G. Mulamoottil,
E.A. McBean, F. Revers (Eds.), Constructed Wetlands for the Treatment of
Landfill Leachates, Lewis Publisher/CRC Press, Boca Raton, Florida, USA, 1999,
pp. 205222.
[66] D. Baldantoni, R. Ligrone, A. Alfani, Macro- and trace-element concentrations
in leaves and roots of Phragmites australis in a volcanic lake in Southern Italy,
J. Geochem. Explor. 101 (2009) 166174.
[67] J. Lehtonen, Effects of acidification on the metal levels in aquatic macrophytes
in Espoo, S. Finland. Ann. Bot. Fennici 26 (1989) 3950.
[68] D. Baldantoni, A. Alfani, P. Di Tommasi, G. Bartoli, A. Virzo De Santo,
Assessment of macro and microelement accumulation capability of two
aquatic plants, Environ. Pollut. 130 (2004) 149156.
[69] B.E.M. Keller, K. Lajtha, S. Cristofor, Trace metal concentrations in the
sediments and plants of the Danube Delta, Romania Wetlands 18 (1998) 42
50.
[70] J. Vymazal, T. Brezinov, Heavy metals in plants in constructed and natural
wetlands: concentration, accumulation and seasonality, Wat. Sci. Tech. 71
(2015) 268276.
[71] S. Clemens, M. Palmgren, U. Krmer, A long way ahead: understanding and
engineering plant metal accumulation, Trends Plant Sci. 7 (2002) 309315.
[72] X.E. Yang, X.X. Long, W.Z. Ni, Physiological and molecular mechanisms of
heavy metal uptake by hyperaccumulating plant species, J. Plant Nutr. Fertil.
8 (2002) 815.
[73] X. Yang, Y. Fengm, Z. Hem, P.J. Stoffelam, Molecular mechanisms of heavy
metal hyperaccumulation and phytoremediation, J. Trace Element Medicine
Biol. 19 (2005) 339353.
[74] D.E. Salt, R.C. Prince, I.J. Pickering, I. Raskin, Mechanisms of cadmium mobility
and accumulation in Indian mustard, Plant Physiol. 109 (1995) 14271433.
[75] Y.P. Tong, R. Kneer, Y.G. Zhu, Vacuolar compartmentalization: a second-
generation approach to engineering plants for phytoremediation, Trends
Plant Sci. 9 (2004) 79.
[76] C.A. Johnston, Sediments and nutrient retention by freshwater wetlands:
effects on surface water quality, CRC Crit. Rev. Environ. Control 21 (1991)
491565.
[77] J. Vymazal, L. Krpfelov, Growth of Phragmites australis and Phalaris
arundinacea in constructed wetlands for wastewater treatment in the Czech
Republic, Ecol. Eng. 25 (2005) 606621.
[78] H. Czkov, Growth dynamics and ecophysiology of Phragmites in relation to
the climatic conditions in boreal-Mediterranean and oceanic-continental
gradients, in: H. Brix (Ed.), Eureed II. Final Project for contracts ENV4-CT95-
0147 and IC20-CT-960020, University of Aarhus, Denmark, 1999, pp. 4552.
[79] K. Soetaert, M. Hoffmann, P. Meire, M. Starink, D. van Oevelen, S. Van
Regenmortel, T. Cox, Modelling growth and carbon allocation in two reed
241
beds (Phragmites australis) in the Scheldt estuary, Aquat. Bot. 79 (2004) 211
234.
[80] L. St-Cyr, P.G.C. Campbell, Metals (Fe, Mn, Zn) in the root plaque of submerged
aquatic plants collected in situ: Relations with metal concentrations in the
adjacent sediments and in the root tissue, Biogeochemistry 33 (1966) 4576.
[81] D.L. Jabob, M.L. Otte, Conflicting processes in the wetland plant rhizosphere:
metal retention or mobilization?, Water Air Soil Pollut 3 (2003) 91104.
[82] K.R. Reddy, R.D. DeLaune, Biogeochemistry of Wetlands. Science and
Application, Taylor & Francis Group, LL, Boca Raton, Florida, 2008.
[83] J. Yang, Z. Ma, Z. Ye, X. Guo, R. Qiu, Heavy metals (Pb, Zn) uptake and chemical
changes in rhizosphere soils of four wetland plants with different radial
oxygen loss, J. Environ. Sci. 22 (2010) 696702.
[84] I.A. Mendelssohn, M.T. Postek, Elemental analysis of deposits on the roots of
Spartina alterniflora Loisel, Am. J. Bot. 69 (1982) 904912.
[85] G.J. Taylor, A.A. Crowder, R. Rodden, Formation and morphology of an iron
plaque on the roots of Typha latofolia L. grown in solution culture, Am. J. Bot.
71 (1984) 666675.
Z.H. Ye, A.J.M. Baker, M.H. Wong, A.J. Willis, Zinc, lead and cadmium
accumulation and tolerance in Typha latifolia as affected by iron plaque on
the root surface, Aquat. Bot. 61 (1998) (1998) 5567.
[87] K.R. Taylor, A.A. Crowder, Use of the DCB technique for extraction of hydrous
iron oxides from roots of wetland plants, Am. J. Bot. 70 (1983) 12541257.
[88] M.L. Otte, J. Rozema, L. Koster, M.S. Haarsma, R.A. Broekman, Iron plaque on
roots of Aster tripolium L.: interaction with zinc uptake, New Phytol. 111
(1989) 309317.
[89] J. Vymazal, L. Krpfelov, Nitrogen and phosphorus standing stock in Phalaris
arundinacea and Phragmites australis in a constructed treatment wetland: 3-
year study, Arch. Agron. Soil Sci. 54 (2008) 297308.
[90] R.W. Howarth, J.M. Teal, Sulfate reduction in a New England salt marsh,
Limnol. Oceanogr. 24 (1979) 9991013.
[91] B. Vigneault, G.C. Campbell, A. Tessier, R. De Vitre, Geochemical changes in
sulfidic mine tailings stored under a shallow water cover, Water Res. 35
(2001) 10661076.
[92] M.O. Doyle, M.L. Otte, Organism-induced accumulation of iron, zinc and
arsenic in wetland soils, Environ. Pollut. 96 (1997) 111.
[93] M.H.M.N. Senden, A.J.G.M. van der Meer, T.G. Verburg, H.T. Wolterbeek, Citric
acid in tomato plant roots and its effect on cadmium uptake and distribution,
Plant Soil 171 (1995) 333339.
[94] A.M. Kinnersley, The role of phytochelates in plant growth and productivity,
Plant Growth Regul. 12 (1993) 207217.
[95] W.E. Rauser, Structure and function of metal chelators produced by plants.
The case for organic acids, amino acids, phytin, and metallothioneins, Cell
Biochem. Biophys. 31 (1999) 1948.
[96] A.R. Memon, P. Schroder, Implications of metal accumulation mechanisms to
phytoremediation, Environ. Sci. Pollut. Res. 16 (2009) 162175.
[97] U. Kramer, J.D. Cotter-Howells, J.M. Charnock, A.J.M. Baker, J.A.C. Smith, Free
histidine as a metal chelator in plants that accumulate nickel, Nature 379
(1996) 635638.
[98] K.M. Evans, J.A. Gatehouse, W.P. Lindsay, J. Shi, A.M. Tommey, N.J. Robinson,
Expression of the pea metallothionein-like gene PsMTA in Escherichia coli and
Arabidopsis thaliana and analysis of trace metal ion accumulation,
implications for PsMTA function, Plant Mol. Biol. 20 (1992)
10191028.
[99] R.H. Kadlec, S.D. Wallace, Treatment Wetlands, second ed., CRC Press, Boca
Raton, Florida, USA, 2009.
[100] L. Krpfelov, J. Vymazal, J. vehla, J. tchov, Removal of trace elements in
three horizontal sub-surface flow constructed wetlands in the Czech
Republic, Environ. Pollut. 157 (2009) 11861194.
[101] B.N. Noller, P.H. Woods, B.J. Ross, Case studies of wetland filtration of mine
wastewater in constructed and naturally occurring systems in Northern
Australia, Wat. Sci. Tech. 29 (1994) 257265.
[102] Z.H. Ye, S.N. Whiting, Z.Q. Lin, C.M. Lytle, J.H. Qian, N. Terry, Removal and
distribution of iron, manganese, cobalt and nickel within a Pennsylvania
constructed wetland treating coal combustion by-product leachate, J.
Environ. Qual. 30 (2001) 14641473.
[103] R.A. Khalid, Chemical mobility of cadmium in sediment-water system, in: J.O.
Nriagu (Ed.), Cadmium in the Environment. Part I, Wiley, New York, 1980, pp.
258304.
[104] P. Adcock, G.G. Ganf, Growth characteristics of three macrophyte species
growing in natural and constructed wetland system, Wat. Sci. Tech. 29 (1994)
95102.
[105] Q. Yang, Z.H. Chen, J.Q. Zhao, B.H. Gu, Contaminant removal of domestic
wastewater by constructed wetlands: effects of plant species, J. Integr. Plant
Biol. 49 (2007) 437446.
[106] J.N.W. Christian, Reed bed treatment systems: experimental gravel beds at
Gravesend the Southern water experience, in: P.F. Cooper, B.C. Findlater
(Eds.), Constructed Wetlands in Water Pollution Control, Pergamon Press,
Oxford, United Kingdom, 1990, pp. 309319.
[107] R. Haberl, R. Perfler, Seven years of research work and experience with
wastewater treatment by a reed bed system, in: P.F. Cooper, B.C. Findlater
(Eds.), Constructed Wetlands in Water Pollution Control, Pergamon Press,
Oxford, UK, 1990, pp. 205214.
[108] A.C. Barbera, G.L. Cirellib, V. Cavallarod, I. Silvestroc, P. Pacificic, V.
Castiglionea, A. Toscanob, M. Milani, Growth and biomass production of
different plant species in two different constructed wetland systems in Sicily,
Desalination 246 (2009) 129136.
242 J. Vymazal, T. Brezinov / Chemical Engineering Journal 290 (2016) 232242
[109] T.R. Headley, L. Davison, D.O. Huett, R. Mller, Evapotranspiration from
subsurface horizontal flow wetlands planted with Phragmites australis in sub-
tropical Australia, Water Res. 46 (2012) 345354.
[110] T.J. Wrigley, D.F. Toerien, The ability of an artificially established wetland
system to upgrade oxidation pond effluent to meet water quality criteria,
Water SA 14 (1988) 171178.
[111] J. Vymazal, P. Krsa, Heavy metals budget for a constructed wetland treating
municipal sewage, in: J. Vymazal (Ed.), Natural and Constructed Wetlands:
Nutrients, Metals and Management, Backhuys Publishers, Leiden, The
Netherlands, 2005, pp. 135142.
[112] T. Brezinov, The seasonal dynamics of heavy metals in vegetation of
constructed wetlands for wastewater treatment (Ph.D. Thesis), Czech
University of Life Sciences Prague, 2015 (in Czech).
[113] J.M. Bernard, T.E. Lauve, A comparison of growth and nutrient uptake in
Phalaris arundinacea L. growing in a wetland and a constructed bed receiving
landfill leachate, Wetlands 15 (1995) 176182.
[114] M. Maddison, K. Soosaar, T. Mauring, . Mander, The biomass and nutrient
and heavy metal content of cattails and reeds in wastewater treatment for
the production of construction material in Estonia, Desalination 246 (2009)
120128.
[115] T. Brezinov, J. Vymazal, Evaluation of heavy metals seasonal accumulation in
Phalaris arundinacea in a constructed treatment wetland, Ecol. Eng. 79 (2015)
9499.
[116] G.A. Di Luca, A.A. Maine, M.M. Mufarrege, H.R. Hadad, G.C. Snchez, C.A.
Bonetto, Metal retention and distribution in the sediments of the constructed
wetland for industrial wastewater treatment, Ecol. Eng. 37 (2011) 1267
1275.
[117] C. Chague-Goff, Assessing the removal efficiency of Zn, Cu, Fe, and Pb in a
treatment wetland using sequential chemical extraction, Water Air Soil
Pollut. 160 (2005) 161179.
[118] C.M. Koretsky, A. Cuellar, M. Haveman, L. Beuving, T. Shattuck, M. Wagner,
Influence of Spartina and Juncus on saltmarsh sediments. II: Trace element
geochemistry, Chem. Geol. 255 (2008) 100113.
[119] B. Sundby, M. Caetano, C. Vale, C. Gobeil, G.W. Luther, D.B Nuzzio, Metal-rich
concretions on the roots of salt marsh sediments, Environ. Sci. Technol. 39
(2005) (2005) 20802086.
[120] P. Sharma, R.S. Dubey, Lead toxicity in plants, Braz. J. Plant Physiol. 17 (2005)
3552.
[121] A. Hanc, D. Baralkiewicz, A. Piechalak, B. Tomoszewska, B. Wagner, E. Bulska,
An analysis of long-distance root to leaf transport in Pisum sativum plants by
laser ablation-ICP-MS, Int. J. Environ. Anal. Chem. 89 (2009) 651659.
[122] P. Eger, Wetland treatment for trace metal removal from mine drainage. The
importance of aerobic and anaerobic processes, Wat. Sci. Tech. 29 (1994)
249256.
[123] J.W. Tonkin, L.S. Balistrieri, J.W. Murray, Modeling sorption of divalent metal
cations on hydrous manganese oxide using the diffuse double layer model,
Appl. Geochem. 19 (2004) 2953.
[124] A. Sobolewski, A review of processes responsible for metal removal in
wetlands treating contaminated mine drainage, Int. J. Phytoremediation 1
(1999) 1951.
[125] L.Y. Lin, Wastewater treatment for inorganics, in: W. Nierenberg (Ed.),
Academic Press, San Diego, 1995, pp. 479484.
[126] J.W. Morse, G.W. Luther, Chemical influences on trace metal-sulfide
interaction in anoxic sediments, Geochim. Cosmochim. Acta 63 (1999)
33733378.
[127] F.M.M. Morel, J.G. Haring, Principles and Applications of Aquatic Chemistry,
Wiley, New York, 1993.
[128] E.P. Achtenberg, C.G.M. Van den Berg, M. Boussemart, W. Davison, Speciation
and cycling of trace metals in Esthwaite water: a productive English lake with
seasonal deep-water anoxia, Geochim. Cosmochim. Acta 61 (1997) 5233
5253.
[129] G. Jin, T. Kelley, N. Vargas, M. Callahan, Preliminary evaluation of metals
removal in three pilot-scale constructed wetland systems, Manage. Environ.
Qual. 14 (2003) 323332.
[130] K.B. Krauskopf, Separation of manganese from iron in sedimentary processes,
Geochim. Cosmochim. Acta 12 (1956) 6184.
[131] B.C. Bostick, C.M. Hansel, M.J.L. Force, S. Fendorf, Seasonal fluctuation in zinc
speciation within a contaminated wetland, Environ. Sci. Technol. 35 (2001)
38233829.
[132] M.L. Otte, C.C. Kearns, M.O. Doyle, Accumulation of arsenic and zinc in the
rhizosphere of wetland plants, Bull. Environ. Contam. Toxicol. 55 (1995) 154
161.
[133] M.A. Huerta-Diaz, R. Caraigan, A. Tessier, Measurement of trace metals
associated with acid volatile sulfides and pyrite in organic freshwater
sediments, Environ. Sci. Technol. 27 (1993) 23672372.
[134] D.B. Kosolapov, P. Kuschk, M.B. Vainshtein, A.V. Vatsourina, A. Wiessner, M.
Kstner, R.A. Mller, Microbial processes of heavy metal removal from
carbon-deficient effluents in constructed wetlands, Eng. Life Sci. 4 (2004)
403411.
[135] B. Hafeez, Y.M. Khanif, M. Saleem, Role of zinc in plant nutrition a review,
Am. J. Exp. Agric. 3 (2013) 374391.
[136] W.G. Hopkins, Introduction to Plant Physiology, second ed., John Wiley &
Sons, New York, 1999.
[137] F.R. Espinoza-Quinones, M.M.T. Fornari, A.N. Mdenes, S.M. Palcio, F. da
Silva Jr, G. Szymanski, A.D. Kroumov, D.E.G. Trigueros, Pollutant removal from
tannery effluent by electrocoagulation, Chem. Eng. J. 151 (2009) 5965.
[138] R.P. Gambrell, Trace and toxic metals in wetlands a review, J. Environ. Qual.
23 (1994) 883891.
[139] M.A. Huerta-Diaz, A. Tessier, R. Carignan, Geochemistry of trace metals
associated with reduced sulphur in freshwater sediments, Appl. Geochem. 13
(1998) 213233.
[140] D. Fibbi, S. Doumett, L. Lepri, L. Checchini, C. Gonnelli, E. Coppini, M. Del
Bubba, Distribution and mass balance of hexavalent and trivalent chromium
in a subsurface, horizontal flow (SF-h) constructed wetland operating as
post-treatment of textile wastewater for water reuse, J. Hazard. Mater. 199
200 (2012) 209216.
[141] S. Soda, T. Hamada, Y. Yamaoka, M. Ike, H. Nakazato, Y. Saeki, T. Kasamatsu, Y.
Sakurai, Constructed wetlands for advanced treatment of wastewater with s
complex matrix from a metal-processing plant: bioconcentration and
translocation factors of various metals in Acorus gramineus and Cyperus
alternifolius, Ecol. Eng. 39 (2012) 6370.
[142] Z. Ben, X. Salem, A. Laffray, H. Ashoour, L. Ayadi Aleya, Metal accumulation
and distribution in the organs of reeds and cattails in a constructed treatment
wetland (Etueffont, France), Ecol. Eng. 64 (2014) 117.
[143] M.N. da Silva, A.P. Mucha, A.C. Rocha, C. Silva, C. Carli, C.R. Gomes, C.M.R.
Almeida, Evaluation of the ability of two plants for the phytoremediation of
Cd in salt marshes, Estuar. Coast. Shelf Sci. 141 (2014) 7984.
[144] M.-Y. Sultana, A.K.M.M.B. Chowdhury, M.K. Michailides, C.S. Akratos, A.G.
Tekerlekopoulou, D.V. Vayenas, Integrated Cr (VI) removal using constructed
wetlands and composting, J. Hazard. Mater. 281 (2015) 106113.
[145] G. Bonanno, Comparative performance of trace element bioaccumulation and
biomonitoring in the plant species Typha domingensis, Phragmites australis
and Arundo donax, Ecotoxicol. Environ. Safety 97 (2013) 124130.
[146] A. Klink, A. Maciol, M. Wislocka, J. Krawczyk, Metal accumulation and
distribution in the ogans of Typha latifolia L. (cattail) and their potential use in
bioindication, Limnologica 43 (2013) 164168.
[147] J. Vymazal, Concentration is not enough to evaluate accumulation of heavy
metals and nutrients in plants, Sci. Total Environ. 544 (2016) 495498.
[148] J. Vymazal, L. Krpfelov, Wastewater Treatment in Constructed Wetlands
with Horizontal Sub-surface Flow, Springer Science + Business Media B.V,
Dordrecht, The Netherlands, 2008.
[149] A. Guittonny-Philippe, V. Masotti, P. Hhener, J.-L. Boudenne, J. Viglione, I.
Laffont-Schwob, Constructed wetlands to reduce meal pollution from
industrial catchments in aquatic Mediterranean ecosystems: a review to
overcome obstacles and suggest potential solutions, Environ. Int. 64 (2014)
116.
[150] J. Teuchies, S. Jacobs, L. Oosterlee, L. Bervoets, P. Meire, Role of plants in metal
cycling in a tidal wetland: implications for phytoremediation, Sci. Total
Environ. 445446 (2013) 146154.
[151] M.J. Van Oosten, A. Maggio, Functional biology of halophytes in the
phytoremediation of heavy metal contaminated soils, Environ. Exp. Bot.
111 (2015) 135146.
[152] N. Fiorentino, M. Fagnano, P. Adamo, A. Impagliazzo, M. Mori, O. Pepe, V.
Ventorino, A. Zoina, Assisted phytoextraction of heavy metals: compost and
Trichoderma effects on giant reed (Arundo donax L.) uptake and soil N-cycle
microflora, Ital. J. Agron. 8 (2013) 244255.
[153] G. Tyler, Distribution and turnover of organic matter and minerals in a shore
meaow ecosystems, Oikos 22 (1971) 25291.
[154] C.J. Richardson, J. Vymazal, Sampling macrophytes in wetlands, in: S.B. Rader,
D.P. Batzer, S.A. Wissinger (Eds.), Bioassessment and Management of North
American Freshwater Wetlands, John Wiley & Sons, New York, 2001, pp. 297
337.
[155] E.M. Eid, K.H. Shaltout, M.A. El-Sheikh, T. Asaeda, Seasonal courses of nutrient
and heavy metals in water, sediment and above- and below-ground Typha
domingensis biomass in Lake Burullus (Egypt): Perspectives for
phytoremediation, Flora 207 (2012) 783794.
[156] J. Vymazal, L. Krpfelov, J. vehla, J. tchov, Can multiple harvest of
aboveground biomass enhance removal of trace elements in constructed
wetlands receiving municipal sewage?, Ecol Eng. 36 (2010) 939945.
[157] H. Lambers, F.S. Chapin III, T.L. Pons, Plant Physiol. Ecol., Springer, New York,
1998.
[158] C.M.R. Almeida, A.P. Mucha, M.T. Vasconcelos, Role of different salt marsh
plants on metal retention in an urban estuary (Lima estuary, NW Portugal),
Estuar. Coast. Shelf Sci. 91 (2011) 243249.