Ecological Engineering 79 (2015) 94–99

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Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Evaluation of heavy metals seasonal accumulation in Phalaris

arundinacea in a constructed treatment wetland
Tereza Brezinová, Jan Vymazal *
Czech University of Life Sciences in Prague, Faculty of Environmental Sciences, Department of Applied Ecology, Kamýcká 129, 165 21 Praha 6, Czech Republic

A R T I C L E I N F O A B S T R A C T

Article history: Constructed wetland for treatment of municipal wastewater was studied with focus on seasonal
Received 20 November 2014 dynamics of heavy metals in the aboveground biomass of Phalaris arundinacea. Aboveground biomass
Received in revised form 6 March 2015 was harvested and evaluated in one or two-month intervals during the period May 2011–March 2012 and
Accepted 6 April 2015
concentrations of Cd, Cr, Cu, Ni, Pb, Zn were determined. Using the heavy metal concentration and
Available online 11 April 2015
biomass values, accumulation as standing stock was calculated for each heavy metal. The results
indicated that maximum standing stock values occurred at different time for each heavy metals. The
Keywords:
results therefore revealed that it is not easy to set the optimum time for aboveground biomass harvest in
Constructed wetlands
Heavy metals
order to remove maximum of all heavy metals at one time. However, it seems that the harvest during the
Phalaris arundinacea early growing season may be the most effective.
Wastewater ã 2015 Elsevier B.V. All rights reserved.

1. Introduction Macrophytes play an important role in wetlands biogeochem-

Constructed wetlands are very complex systems that are used
for wastewater treatment, especially for domestic and municipal
sewage. Until now, these systems have been extensively monitored
with focus on removal of organics, suspended solids, nutrients and
microorganisms (Vymazal and Kröpfelová, 2008), whereas knowl-
edge about the metals removal is still limited (e.g., Peverly et al.,
1995; Lesage et al., 2007a; Bragato et al., 2009; Yeh et al., 2009).
Heavy metals often do not constitute the main problem in
municipal wastewater because the concentrations of heavy metals
are usually low, namely in wastewaters from small municipalities
with no industrial effluents (e.g., Vymazal et al., 2007; Kröpfelová
et al., 2009). However, heavy metals tend to accumulate in
sediments and plants; the amount sequestered in the sediments
increase with operation time of constructed wetlands (Scholes
et al., 1998; Vymazal and Krása, 2005; Vymazal et al., 2010a;
Ranieri and Young, 2012). The elevated concentrations of heavy
metals in the sediments may subsequently cause higher uptake by
plants and sequestration of heavy metals into plant biomass. In
addition, the application of constructed wetlands for industrial and
agricultural wastewaters with elevated heavy metals concentra-
tions has recently drawn increased attention (Maine et al., 2006;
Khan et al., 2009) and, therefore it is desirable to focus on the role
of macrophytes in heavy metals cycle in constructed wetlands.
* Corresponding author. Tel.: +420 22438 3825.
E-mail address: vymazal@knc.czu.cz (J. Vymazal).
istry thanks their passive and active circulation of elements
(Tanner, 1996; Weis and Weis, 2004). The concentrations of heavy
metals in wetland plants growing in constructed and natural
wetlands usually decrease in the order roots > rhizomes  leaves >
stems (e.g., Schierup and Larsen, 1981; Peverly et al., 1995;
Windham et al., 2003; Zhang et al., 2009; Maddison et al., 2009;
Vymazal et al., 2010b; Bonanno, 2011). However, the concentration
itself does not provide the information about accumulation of
heavy metals in the plant biomass. The accumulation of heavy
metals in plants in constructed and natural wetlands heavily
depends on the amount of biomass. Due to substantially
higher aboveground than belowground biomass in constructed
wetlands (e.g., Behrends et al., 1994; Bernard and Lauve, 1995;
Peverly et al., 1995), the accumulation of heavy metals is
frequently higher in the aboveground biomass despite lower
concentrations in the aboveground biomass (Cardwell et al., 2002;
Bhattacharya et al., 2006).
Although the results have shown that the amount of heavy
metals sequestered in the aboveground biomass contributes to the
overall removal is limited, identification of the period that
corresponds with the maximum accumulation of heavy metals
in the aboveground biomass is important in view of optimizing the
removal through biomass harvest (Bragato et al., 2009). The
information about the seasonal fluctuation of heavy metals
concentrations in the aboveground vegetation in plants growing
in natural (e.g., Tyler, 1971; Larsen and Schierup, 1981; Windham
et al., 2003; Baldantoni et al., 2009) and constructed (e.g., Bernard
and Lauve, 1995; Bragato et al., 2009; Galletti et al., 2010) wetlands

http://dx.doi.org/10.1016/j.ecoleng.2015.04.008
0925-8574/ ã 2015 Elsevier B.V. All rights reserved.
 T. Brezinová, J. Vymazal / Ecological Engineering 79 (2015) 94–99
has often been reported in the literature. However, the information
on seasonal fluctuation of heavy metal accumulation in the
aboveground biomass of wetland plants has been reported only
seldom in natural wetlands (e.g., Tyler, 1971; Larsen and Schierup,
1981; Kufel, 1991; Windham et al., 2003) and only few results have
been published from constructed wetlands (e.g., Behrends et al.,
1994; Bernard and Lauve, 1995; Maddison et al., 2009).
Total accumulation of an element in a particular compartment
is called standing stock (Brock et al., 1983; Twilley et al., 1985;
Johnston, 1991). Standing stocks in the vegetation are commonly
computed by multiplying nutrient concentrations in the plant
tissue by biomass per unit area and are expressed as mass per unit
area (usually g m 2 or kg ha 1) (Richardson and Vymazal, 2001).
Therefore, both biomass amount and heavy metal concentrations
are important for standing stock determination. In temperate and
cold climates, the seasonality of nutrient standing 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 (Tyler, 1971; Richardson and Vymazal, 2001). On
the other hand, the standing stock seasonality for heavy metals
varies among metals and there is no uniform pattern (Tyler, 1971;
Vymazal and Kröpfelová, 2008).
The aim of this study was (a) to evaluate the seasonal pattern of
heavy metals accumulation in the aboveground biomass of Phalaris
arundinacea in a constructed wetland and (b) to evaluate the
optimum time for vegetation harvesting for maximum removal of
heavy metals from wastewater.
 cenice; (A) October 2010, (B) May 2011, (C) June 2011, (D) February 2012 (photo authors).
Fig. 1. Constructed wetland in Cí9
95
2. Materials and methods
Constructed wetland Cì9 cenice, South Bohemia, Czech Republic,
was designed for treatment of municipal sewage from 450 PE. The
system consists of mechanical pretreatment (screens, grit chamber
and Imhoff tank) with four equally sized beds filled with washed
gravel (8–16 mm) with a total area of 2400 m2. The system was
planted with Reed canarygrass (P. arundinacea) in 2010 and
provided full vegetation cover in 2011 (Fig. 1). The average air
temperatures at the site were 9.7  C and 9.5  C in 2011 and 2012,
respectively. The lowest and highest average monthly temper-
atures during the monitored period were 4  C (February 2012)
and 18.5  C (August 2011). The average inflow and outflow
concentrations of monitored heavy metals, BOD5, COD and TSS
are given in Table 2.
The research was carried out in one bed and the aboveground
biomass of P. arundinacea was harvested in May June, July, August,
September and November 2011 and January and March 2012 in the
inflow and outflow zones of the filtration bed. The aboveground
biomass was clipped at the ground level from 0.25 m2 quadrants in
four replicates both in inflow and outflow zones. The biomass was
separated into leaves (including leaf sheaths), stems and flowers (if
present) and dried at 60  C to a constant weight and weighed. The
biomass was then homogenized using a cutting mill (Pulverisette
15, FRITSCH) and mineralized in nitric acid (Ultrapur, Merck
Millipore) in a microwave (Berghof, Speedwave MWS-2) under
high temperature and pressure. The concentrations of heavy
96 T. Brezinová, J. Vymazal / Ecological Engineering 79 (2015) 94–99

September until March 2012 (0.27 mg m 2). This observation is in

Fig. 2. The average amount of aboveground biomass in constructed wetland
 cenice during the period May 2011–March 2012. Different letters indicate
Cí9
significant difference at a = 0.05 between the means.
metals (Cd, Cr, Cu, Ni, Pb, Zn) in leaves, stems and flowers were
determined in triplicate samples using the atomic absorption
spectroscopy (Agilent AAS DUO 55B/240Z). For the evaluation of
measurement precision and accuracy the certified reference
material (CRM) METRANAL TM3 (Fragaria vesca, QCM03, Analytica
Ltd., Czech Republic) was used. The triplicate determinations
agreed to within 5%, and CRM recoveries were found within
90–105% range. Heavy metal standing stocks (SS) were calculated
as follows: SS (mg m 2) = concentration (mg kg 1)  dry matter
(kg m 2). Standing stock was calculated for each plant part
separately (leaf, stem, flower) and total aboveground standing
stock was a sum of these partial standing stocks. For statistical
analyses, Turkey HSD test (p < 0.05) was used.
3. Results and discussion
accordance with results reported by Windham et al. (2003) for
Phragmites australis growing in New Jersey natural marsh, Bernard
and Lauve (1995) for P. arundinacea growing in a natural wetland in
New York State and T. domingensis growing in the Lake Burullus in
Egypt (Eid et al., 2012). On the other hand, Tyler (1971) observed a
steady increase of lead standing stock in several wetland plants in a
natural wetland located south of Stockholm, Sweden during the
period March–November. The pattern was observed by Kufel
(1991) in P. australis growing in a eutrophic lake in Poland during
the period June–October. On the other hand, lead standing stock in
Typha angustifolia remained steady throughout this monitoring
period. These results may indicate that lead standing stock
in various plants follows a different pattern throughout the
season. The maximum values of lead standing stock found
during the monitored period are well within the range reported
from both natural and constructed wetlands for various wetland
plants (Table 1).
3.2.3. Nickel
Nickel standing stock seasonal pattern in P. arundinacea (Fig. 4)
exhibited the highest values in the beginning of the growing
season in May (1.62 mg m 2). The standing stock values then
dropped down throughout the summer and then remained more
or less steady until March 2012. Tyler (1971), however, observed a
steady increase in nickel standing stock in several wetland plants
in Sweden during the period March–November. The maximum
value observed in our study was comparable with values reported
for P. australis by Lesage et al. (2007b) from a hybrid constructed
wetland Zevergem, De Pinte in Belgium, but lower if compared to
the value reported by Vymazal et al. (2010b) for P. arundinacea in a

3.1. Aboveground biomass

The average aboveground biomass harvested during the period

May 2011–March 2012 is shown in Fig. 2. The amount of biomass
increased throughout the growing season and peaked in July, the
typical time for peak biomass for P. arundinacea in the Czech
Republic (Vymazal and Kröpfelová, 2005). The aboveground
biomass then remained steady during the summer and started
to decrease in the autumn with the lowest biomass recorded in the
March 2012. The maximum recorded biomass (1168 g m 2) close to
the average maximum biomass for P. arundinacea in Czech
constructed wetlands (1286 g m 2) reported by Vymazal and
Kröpfelová (2005).

3.2. Seasonal pattern of heavy metal accumulation

3.2.1. Cadmium
The maximum cadmium standing stock of (0.15 mg m 2) was
recorded in July (Fig. 3) and since then it decreased steadily until
March when the standing stock value of 0.02 mg m 2 was recorded.
Eid et al. (2012) reported a very similar seasonal pattern for
cadmium standing stock in aboveground biomass of Typha
domingessis in Egypt with the peak standing stock occurring in
July at the time of the peak biomass. The range of standing stock
values found in our study were within the range (0.002–0.2 mg
m 2) reported in the literature for various plants in constructed
wetlands (Table 1).

3.2.2. Lead
Lead standing stock (Fig. 3) exhibited similar seasonal pattern
as cadmium and the highest stock of 0.82 mg m 2 was recorded in
June and, after a short steady stage, it started to decrease since
Fig. 3. Average standing stocks of cadmium (top) and lead (bottom) in the
aboveground biomass of Phalaris arundinacea during the period May 2011–March
2012 in CW Cí9  cenice. Different letters indicate significant difference at
a = 0.05 between the means.
 T. Brezinová, J. Vymazal / Ecological Engineering 79 (2015) 94–99 97

Table 1
Accumulation of heavy metals as standing stock (mg m 2) in the aboveground biomass of wetlands plants in constructed and natural wetlands. HF CW – horizontal subsurface
flow constructed wetland, VF CW = vertical flow constructed wetlands, FWS CW = free water surface constructed wetland.

Plant Location Cd Pb Ni Cu Zn Cr
1 Phalaris arundinacea FWS CW USA 0.2 0.6–3.2 2.3–16.9
2 Phalaris arundinacea Czech 0.014 1.32 5.97 8.81 28.5 0.54
HF CW Republic
3 Phragmites australis Belgium 0.038 0.36 0.57 2.9 30 0.57
HF CW
4 Phalaris arundinacea USA 0.76–2.0 6.6–14.8
HF CW
3 Phragmites australis Belgium 0.014 0.44 0.91 7.5 90 0.6
VF CW
5 Phragmites australis USA 0.057 0.10 3.2 18.4
HF CW
6 Phragmites australis Italy 3.23 9.19 90.3
HF CW
4 Phragmites australis USA 3.5–5.7 22-81
HF CW
7 Typha latifolia Estonia 0.002–0.2 0.02–0.6 0.2–9.2 1.1-53.7
FWS CW
4 Typha spp. USA 0.8–1.9 5.2-12
HF CW
1 Phalaris arundinacea USA 0.1–1.1 0.5–3.6 2.0-21

Natural stand
8 Phragmites australis Natural stand USA 0.05–1.1 0.4–4.4 1.6–49 0.06-1.1
9 Phragmites australis Denmark <0.08 <0.8 1.0–1.5 14–26
Two lakes
10 Phragmites australis Poland 2.53
Eutrophic lake
10 Typha angustifolia Eutrophic lake Poland 0.03

1-Bernard and Lauve (1995), 2-Vymazal et al., (2010b), 3-Lesage et al. (2007b), 4-Behrends et al. (1994), 5- Peverly et al. (1995), 6- Galletti et al. (2010), 7-Maddison et al.
(2009), 8-Windham et al. (2003), 9- Schierup and Larsen (1981), 10-Kufel (1991).

constructed wetland Brehov in the Czech Republic. Also Galletti steady decrease in copper standing stock for Scirpus acutus
et al. (2010) reported higher standing stock in constructed throughout the growing season. The results shown in Table 1
wetlands in Ferrara, Italy (Table 1). indicated that standing stock values found in our study are lower if
compared to most values reported in the literature.
3.2.4. Copper
Copper also exhibited the highest standing stock (1.13 mg m 2)
3.2.5. Zinc
early in the growing season (Fig. 4). After that, the standing stock
The seasonal pattern of zinc standing stock (Fig. 5) exhibited the
decreased but increased again in January and March. The same
highest value in June but in general, it remained very steady during
seasonal pattern of copper standing stock was reported by Tyler
the monitored period. The standing stock varied only between
(1971) for several wetland plants in Sweden. Also Behrends et al.
7.89 mg m 2 in June and 4.96 mg m 2 in March. The seasonal
(1994) observed the same pattern for P. arundinacea and P. australis
pattern is in accordance with that reported by Tyler (1971) for
in a HF constructed wetland in Alabama. However, in the same
several wetland plants in Sweden but other studies reported
experiment, copper standing stock gradually increased throughout
different seasonal patterns. Windham et al. (2003) observed a
the period of June–November for Scirpus cyperinus,S. atrovirens and
steady increase in Zn standing stock in P. australis between April
Typha spp. The same pattern was observed by Windham et al.
and October while and Behrends et al. (1994) reported a steady
(2003) in P. australis in a natural wetland in New Jersey during the
increase for P. australis, S. cyperinus, S. atrovirens and Typha spp.
period of April–October. On the other hand, Eid et al. (2012)
During the period June–November. Eid et al. (2012), on the other
reported a steady increase of copper standing stock in
hand, observed a clean peak zinc standing stock value in July for
T. domingensis in Egypt from February to July up to the value of
T. domingensis in Egypt and the same pattern was observed by
about 55 mg m 2 followed by steady decrease until October. In
Behrends et al. (1994) for S. acutus in Alabama. The data presented
contrast to all mentioned studies, Behrends et al. (1994) reported a
in Table 1 indicated that zinc standing stock measured in our study
are lower as compared to values reported in the literature.
Table 2
Average inflow and outflow concentrations of monitored heavy metals during the
period 5/2011-3/2012 (n = 8) and average concentrations of BOD5, COD and TSS 3.2.6. Chromium
during the period 1/2011-12/2012 (n = 8, data obtained from the local municipality). Chromium standing stock in P. arundinacea (Fig. 6) exhibited a
Inflow Outflow Removal Inflow Outflow Removal
unique seasonal pattern which differed from all other studied
(mg l 1) (mg l 1) (%) (mg l 1) (mg l 1) (%) heavy metals. The standing stock values in the beginning of the
BOD5 82 8.5 90 Zn 26.4 12.8 52
growing season (May, June) were followed by a decrease in July and
COD 187 39 79 Cu 5.7 3.8 33 the increase again with the peak standing stock occurring in
TSS 71 16 77 Pb 4.5 3.2 29 September (Fig. 6). After September, the standing stock values
Ni 2.8 2.1 25 decreased slightly but remained higher than those found in the
Cr 0.91 0.75 18
beginning of the growing season. Windham et al. (2003) reported
Cd 0.81 0.73 10
quite opposite seasonal pattern for P. australis with increase in
98 T. Brezinová, J. Vymazal / Ecological Engineering 79 (2015) 94–99

Fig. 6. Average standing stocks of chromium in the aboveground biomass of

Phalaris arundinacea during the period May 2011–March 2012. Different letters
indicate significant difference at a = 0.05 between the means.

Table 3
Minimum and maximum heavy metal standing stocks and time of respective
occurrence during the monitored period (May 2011–March 2012). In parentheses,
minimum standing stock values as percentage of maximum values.
2
Standing stock (mg m ) Month

Minimum Maximum Minimum Maximum

Cadmium 0.02 (13%) 0.153 March July
Lead 0.27 (33%) 0.82 March August
Nickel 0.42 (26%) 1.62 March May
Copper 0.68 (60%) 1.13 September May
Zinc 4.96 (68%) 7.37 March May
Chromium 0.14 (54%) 0.26 July September

Fig. 4. Average standing stocks of nickel (top) and copper (bottom) in the
aboveground biomass of Phalaris arundinacea during the period May 2011–March
2012. Different letters indicate significant difference at a = 0.05 between the means.
standing stock in June and lower values before and after that. The
peak standing stock value found in our study was lower that values
reported in the literature (Table 1).
3.2.7. All monitored heavy metals
The results of the present study indicated that seasonal
distribution of heavy metals in the aboveground biomass of
P. arundinacea varies among metals and there is no clear seasonal
pattern. Moreover, available literature data revealed that seasonal
pattern and time of maximum standing stock for individual heavy
metals may differ. However, the results presented in Table 3
suggest that the minimum standing stock, i.e., the lowest
accumulation of heavy metals occurs in March in the senescent
plant tissues due to low biomass (Fig. 2). Biomass is the factor
which determines the value of standing stock (Richardson and
Vymazal, 2001). Despite the low biomass in May (Fig. 2), three
heavy metals (Ni, Cu, Zn) exhibited the highest accumulation at
this time (Table 3) indicating high rate of uptake and subsequent
translocation from roots to shoots in the early growing season. The
data shown in Table 3 indicated that the harvest in appropriate
time can substantially increase the removed amount of heavy
metals. It is obvious that further research is necessary to optimize
vegetation harvesting for heavy metal removal in constructed
wetlands.

4. Conclusions

Fig. 5. Average standing stocks of zinc in the aboveground biomass of Phalaris
arundinacea during the period May 2011–March 2012. No statistical difference were
found among monthly means.
The results obtained during this study have shown that heavy
metals accumulation in the aboveground biomass of P. arundinacea
growing in a constructed wetland treating municipal sewage varies
substantially during the season and also among heavy metals. It
seems 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 maximum removal of all heavy
metals at the same time. Despite low aboveground biomass in the
early growing season, some heavy metals exhibited the highest
level of accumulation at this time. Appropriate time for harvest
may optimize removal of heavy metals in constructed wetlands.
 T. Brezinová, J. Vymazal / Ecological Engineering 79 (2015) 94–99 99

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