- Email: [email protected]
Integration of phytogreen for heavy metal removal from wastewater
Accepted Manuscript Integration of Phytogreen for heavy metal removal from wastewater A.R. Abdul Syukor, S. Sulaiman, Md. Nurul Islam Siddique, A.W. Zularisam, M.I.M. Said PII:
S0959-6526(15)01575-9
DOI:
10.1016/j.jclepro.2015.10.103
Reference:
JCLP 6334
To appear in:
Journal of Cleaner Production
Received Date: 25 January 2015 Revised Date:
23 October 2015
Accepted Date: 24 October 2015
Please cite this article as: Syukor ARA, Sulaiman S, Siddique MNI, Zularisam AW, Said MIM, Integration of Phytogreen for heavy metal removal from wastewater, Journal of Cleaner Production (2015), doi: 10.1016/j.jclepro.2015.10.103. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
b
M AN U
SC
RI PT
a
d
EP
TE D
c
Fig. SEM of (a, c) heavy metals loaded dried (Thypha angustifolia) biomass (b, d) heavy metals loaded
AC C
dried (Limnocharis flava) biomass ×100 and 500.
The Graphical Abstract.
1
ACCEPTED MANUSCRIPT
Integration of Phytogreen for heavy metal removal from wastewater
*
E-mail: [email protected]
RI PT
A.R. Abdul Syukora*, S. Sulaimana, Md. Nurul Islam Siddiqueb, A. W. Zularisamb, M.I.M. Saidc
Tel: +60 9 5492931; Fax: +60 9 5492998 a
Faculty of Civil Engineering and Earth Resources, University Malaysia Pahang (UMP), Lebuhraya Tun
b
SC
Razak, 26300 Gambang, Kuantan, Pahang, Malaysia.
Faculty of Engineering Technology, University Malaysia Pahang (UMP), Lebuhraya Tun Razak, 26300
c
M AN U
Gambang, Kuantan, Pahang, Malaysia.
Faculty of Civil Engineering, Universiti Teknologi Malaysia (UTM), 81310 University Technology Malaysia Skudai, Johor, Malaysia.
Abstract
TE D
Although the oxidation pond process for the treatment of wastewater has been widely studied and commercial application has already been recognized, the integration of the phytogreen system has yet to be studied. This work was focused on investigating the improvement in the conventional oxidation pond process produced by the integrated phytogreen system for the treatment of wastewater. Among the
EP
conventional treatment systems, the phytogreen integrated oxidation pond process appears to be an efficient system, affecting the bio-removal of heavy metals. The influence of the integrated Phytogreen system,
AC C
including two different aquatic plants (Typha angustifolia sp. and Limnocharis flava sp.) in the conventional oxidation pond process, was investigated for a retention time of 13 days. The results revealed that the integrated Phytogreen system realized the maximum removal of copper to 79.07%, magnesium to 68%, cadmium to 61.07%, chromium to 69.17%, nickel to74.87%, iron to 81.17%, lead to 62.07% and zinc to 63% at a retention time of 13 days when the two plant species were combined together. A positive relation between retention time and heavy metal removal was studied, and it was confirmed by the negative and significant correlation coefficients of the corresponding heavy metals with retention period. The results revealed that the integrated phytogreen system consisting of two different aquatic plants (Typha angustifolia
1
ACCEPTED MANUSCRIPT
sp. and Limnocharis flava sp.) in the conventional oxidation pond process is a reliable and ecologically attractive option. Finally, integration of Phytogreen is proposed to minimize heavy metal contamination in wastewater.
RI PT
Keywords: Retention time, wastewater, Phytogreen, heavy metal removal.
1. Introduction
A range of commercial activities such as mining, plating, dyeing, automobile manufacturing and metal
SC
processing are responsible for heavy metal contamination of our environment (Matouq et al., 2015). This contamination has introduced numerous environmental problems (Zhu et al., 2015). The proper monitoring
M AN U
of heavy metals in wastewater is obligatory for maintaining water and food quality standards (Han et al., 2015).
Protection of the environment is one of the key concerns of this century (Smain et al., 2009). In particular, the discharge of natural or synthetic materials is one of the most substantial factors contributing to the degradation of the biosphere (Siddique et al., 2014). Aquatic environments are the end destinations of these substances, and they frequently carry high concentrations of pollutants that may be toxic for organisms
TE D
(Rodolfo et al., 2015). Among these polluting substances, heavy metals are easily transported and accumulated in the environment (Byungryul et al., 2015). They reach aquatic environments as dissolved and solid waste from domestic, industrial, and agricultural runoffs (Smain et al., 2009).
EP
The discharge of inadequately treated municipal sewage and industrial waste containing heavy metals into waterways has become a severe environmental issue for the civilization (Siddique et al., 2014). The use of
AC C
heavy metal-contaminated water poses a hazard to public health (Akcil et al., 2015). Removal of heavy metals by conventional chemical treatment methods such as precipitation, coagulation–flocculation, adsorption, ion exchange, membrane filtration and other advanced oxidation processes involves huge operational and supervision costs (Lara et al., 2014). Therefore, it has become obligatory to recommend a cost-effective green technology to eliminate these heavy metals and improve the effluent standard (González et al., 2014). Integration of Phytogreen in heavy metal removal from wastewater has numerous advantages. Aquatic plants are able to act as natural absorbers of heavy metals and other contaminants (Pratas et al., 2014).
2
ACCEPTED MANUSCRIPT
Elimination of heavy metals and other contaminants from wastewater by aquatic plants has been recommended as the most economic and efficient method (Philippe et al., 2014). In the past few decades, aquatic plants or fabricated wetlands were applied widely for the elimination of heavy metals and
RI PT
contaminants from wastewater (Mesa et al., 2015). Among aquatic plants, emergent plants are capable of accumulating metals in their tissues over several times the concentration of that in the adjacent environment, which may be caused by metal uptake of the plants through adsorption to anionic sites in the cell walls (Deng et al., 2014). However, integration of Phytogreen technology in heavy metal removal from
SC
wastewater is time consuming (Syukor et al., 2013). The cultivation and growth of the aquatic plants usually takes a significant amount time, which may be a disadvantage of this technology (Said et al., 2015).
M AN U
However, the disadvantages of this green technology can be offset by its numerous advantages (Syukor et al., 2014).
Typha angustifolia sp. and Limnocharis flava sp. are recognized hyper-accumulator emergent plants (Rezania et al., 2015). These plants grow in marshlands and sedge meadows and along slow-moving streams, river banks, and lake shores. These two plants are found in regions of fluctuating water levels such
TE D
as roadside ditches, reservoirs and other disturbed wet soil areas. Typha angustifolia sp. is usually limited to unstable surroundings, habitually with basic, calcareous, or somewhat salty soils (Fassett and Calhoun 1952). Cattail can grow in deep water compared with Typha angustifolia sp., although both plants can
EP
achieve maximum growth at a water depth of 50 cm (20 inches) (Grace and Wetzel 1981). The tolerance of Typha angustifolia sp. to high concentrations of lead, zinc, copper, and nickel has been established (Taylor
AC C
and Crowder 1984). This species has been used in secondary wastewater treatment schemes (Gopal and Sharma 1980) and has been observed in most suitable sites where it contests against other species. Typha angustifolia sp. and Typha domingensis sp. are limited to less favorable and more saline environments when they grow with Typha latifolia sp. (Gustafson 1976). Typha latifolia sp.
often replaces Typha angustifolia
sp. in shallow (\<15 cm) depths, limiting the other species to deep water (Grace and Wetzel 1981). Typha
angustifolia sp. is believed to be a pioneer species for secondary succession of disturbed bogs (Wilcox et al. 1984). Apparently, an incremental change in the acidity of a bog decreases both the pH and the incursion of Typha angustifolia sp. According to Theodore Cochran (pers. comm.) of the University of Wisconsin-
3
ACCEPTED MANUSCRIPT
Madison herbarium, most early herbarium specimens are Typha latifolia sp., and only recently have Typha angustifolia sp. been collected from Wisconsin wetlands. In 1962, Smith was the first to report on the heavy metal removal efficiency of these plants. These two plants can accumulate heavy metals such as copper,
RI PT
cadmium, chromium, nickel and lead at levels of up to 0.1% and iron and zinc at levels of up to 1% of the plant dry weight (Ponce et al., 2015). Several studies have been carried out on the metal removal performance of these two plants (Chandra and Yadav in 2010; Bah et al., in 2010; Xu et al., in 2011; Liu et al., in 2011 and Abhilash et al., in 2009). However, these particular plants are not being used for heavy
SC
metal elimination commercially. There is still a huge scarcity of data confirming the contributions of Typha angustifolia and Limnocharis flava when cultivated together for the elimination of heavy metals. Although
M AN U
the oxidation pond process for the treatment of wastewater has been widely studied and commercial application has already been recognized, the integration of the phytogreen system has yet to be studied. Consequently, this manuscript may help meet the increasing demand of society for heavy metal removal. Therefore, the key objectives of the present study were to determine the heavy metal removal efficiency of the integrated Phytogreen system consisting of two different aquatic plants, namely, Typha angustifolia sp. and Limnocharis flava sp., in the conventional oxidation pond process and the relationship between the
TE D
retention time and heavy metal removal.
2. Materials and Methods
EP
Raw municipal sewage and industrial wastewater were obtained from four sampling stations (S1-S4) along the 12 km of Karteh, Malaysia (6° 5' 59N, 100° 21' 6E) and transported to the laboratory for experimental
AC C
use. To minimize error during sampling, each sample was obtained separately and used as four discrete replicates.
Batch tests were carried out with similar samples obtained during similar phases.
Characterization of the obtained samples is shown in Table 1. Typha angustifolia and Limnocharis flava
were collected from the Gebeng industrial area and Pekan of Malaysia.
2.1. Experimental Setup The integrated phytogreen system consisted of five zones: the influent zone (Z1), the Phytogreen zone (Z2), the aeration zone (Z3), the inclined plate clarifier zone (Z4) and the effluent zone (Z5) (Fig. 1). Each
4
ACCEPTED MANUSCRIPT
phytogreen system zone had a capacity of 75 L and was connected with a 20 PVC pipe that had a diameter of 5 cm and pores with a diameter of 25 mm to ensure fluid exchange. While performing this work, Typha angustifolia sp. and Limnocharis flava sp. plants of 34.4±1.5 cm in length and 44.6±0.4 g in weight were
RI PT
chosen and planted in the phytogreen zone. Phase 1 consisted of only Typha angustifolia sp. at a density of 30 plants per m2. Phase 2 consisted of only Limnocharis flava sp. at a density of 30 plants per m2. During phase 3, both Typha angustifolia sp. and Limnocharis flava sp. were planted at a density of 15 plants per m2. Phase 4 was treated as a control group (without plants) for the determination of heavy metal removal by
SC
nature.
M AN U
2.2. Operational design
Acclimatization of the selected plants was carried out using distilled water for 7 days; the selected plants were cleaned properly with distilled water before being used in the phytogreen zone. Then, 60 L of raw wastewater obtained from the four different stations (S1-S4) was fed to each of the experimental phases and subjected to 10 hours of sunlight. Double-distilled water was used to balance the evaporation loss at a fixed interval; the pH of the wastewater remained fixed, as a small amount of double distilled water was added to
Fig. 1 and Fig. 2.
EP
2.3. Methods
TE D
balance the amount lost. A schematic drawing and photograph of the total experimental setup are shown in
Samples were obtained individually starting from the first to 13th day of treatment from the four individual
AC C
experimental phases: S1-S4. pH, COD, BOD, total nitrogen and P for inflowing and outgoing waste were analyzed using standard procedures (APHA, 2005). The concentrations of heavy metals were analyzed through a scheme of sequential extraction according to the procedure of Nguyen and Lee (2014). ICP-OES was applied to analyze the concentration of heavy metals in the extracted liquor during the sequential extraction processes.
5
ACCEPTED MANUSCRIPT
2.4. Statistical Analysis A Kolmogorov–Smirnov (K–S) test was used to investigate the normality of the obtained data. A 3-way analysis of variance (ANOVA) was carried out to assess the effect of the plants, heavy metal concentrations
RI PT
and retention times on the removal of heavy metals. To determine the differences among the averages, a Duncan multiple range test (alpha = 0.05) was carried out. Correlation between the heavy metal level and retention time was determined by Spearman rank order correlation.
The Spearman rank coefficient is analyzed based on two criteria: (a) the variables should be intervals or
SC
ratios, and (b) a monotonic relationship exists between them. Both criteria were fulfilled; the retention time and heavy metal concentrations were interval variables and monotonic relationship existed between them.
% removal efficiency =
M AN U
The heavy metal removal percentage was obtained using the following equation:
Ci - Cf X 100 Ci
(1)
Where, Ci and Cf are the initial and final heavy metal concentrations.
TE D
3. Results and Discussion
The effect of the plants, pH and retention time on the removal of heavy metals is explained clearly in this section.
EP
3.1. Performance of plants on heavy metal removal To assess the performance of the selected plants in the removal efficiency of heavy metals, Typha
AC C
angustifolia sp. and Limnocharis flava sp. were cultivated separately and together. Analysis of variance and the Duncan multiple range test (p = 0.05) suggested the maximum removal of Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd for combined culture of Typha angustifolia sp. and Limnocharis flava sp. and minimum removal for Typha angustifolia sp. (Table 2). However, the results revealed that the integrated Phytogreen system
realized the maximum removal of Cu to 79.07%, Mg to 68% Cd to 61.07%, Cr to 69.17%, Ni to74.87%, Fe to 81.17%, Pb to 62.07% and Zn to 63% at a retention time of 13 days when two plants were combined together. Identical results for the enhancement of arsenic and heavy metal removal efficiency from wastewater using a combined culture of A. ferrooxidans and A. thiooxidans was found by Nguyen and Lee in
6
ACCEPTED MANUSCRIPT
2015. The current results are also reinforced by Marchand et al. (2014) during treating wastewater by plants. When Typha angustifolia sp. and Limnocharis flava sp. were cultivated separately and together, the heavy metal removal was increased by the metal uptake of the plants. The uptake methods involve precipitation
RI PT
and co-precipitation (Ladislas et al., 2014). Typha angustifolia sp. and Limnocharis flava sp. provided food and an environment suitable for the propagation of microbes through their rhizosphere, which are the key locations for heavy metals immobilization and uptake by these plants (Mendoza et al., 2015). The combined application of Typha angustifolia sp. and Limnocharis flava sp. indicated that the maximum uptake
SC
efficiency was due to the increase in their rhizospheres. Moreover, the enhanced rhizosphere may help to increase the uptake efficiency of the cell. The defecation of phytosiderophores by the plants results in a
performance (Hu et al., 2014).
M AN U
complex with free heavy metal ions that might be considered a secondary cause for the increase in uptake
The favored order for heavy metal removal was Fe> Ni> Cu> Zn> Cr> Pb> Mg> Cd when the combined culture of Typha angustifolia sp. and Limnocharis flava sp. was employed. While performing phytoremediation of contaminated soil, a similar trend of metal uptake was observed by Oosten and Maggio in 2015. This current method was able to achieve greater Cd and Zn removal from S4 wastewater (49.3%
TE D
and 59.6%) than that observed by Ahmadi et al. (2014) while treating aqueous solutions with maghemite nanoparticles (20% and 52%) (Table 2). Similarly, for Cr removal, the present method showed greater removal efficiency from S4 wastewater (58.3%) than those studied by Ceglowski and Schroeder (2015)
EP
while treating aqueous solutions with a porous resin (Table 2). The greater removal of Cd, Zn and Cr may be due to the plants' greater uptake efficiency of metals when compared with the oxidation process and other
AC C
advanced technologies. Sargın et al. (2015), using pollen–chitosan microcapsules, observed lower removal of Cd (26.6%), Cu (40.8%), Ni (16.2%) and Zn (21%) compared with the findings of the present work. Noticeably, the present work achieved greater Fe removal (81.17%) than that of Shavandi et al. (2012) during POME treatment with natural Zeolite. While treating heavy metal contaminated soil with Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis, Babu et al. (2015) found 36% Zn,
40% Pb and 68% Cu removal, which are 27%, 22.07% and 11% less than our findings. Morteza et al. (2015) examined heavy metal removal efficiency from aqueous solutions using sunflower, potato, canola and walnut shell residues and found that the nickel removal efficiency was approximately 55%, while the present
7
ACCEPTED MANUSCRIPT
work achieved a higher nickel removal efficiency of 62.2% when two plants (Typha angustifolia sp. and Limnocharis flava sp.) were applied together. Mohammad et al. (2015) carried out an experiment on the uptake of heavy metals by maize plants and achieved 21.2% Zn and 29% Cu removal, while this work
3.2. Relation of pH and heavy metal removal
RI PT
achieved 38.4% and 32.8% higher removal for Zn and Cu.
The relation between pH and heavy metal removal was studied by measuring pH and heavy metal density
SC
over the course of the experiment. Primarily, the pH of the S4 wastewater was alkaline in nature. Subsequently, variation in the pH from 6.85±0.01 to 7.79±0.01 was observed. This change in pH may be due
M AN U
to the addition of O2 via the disintegration of the atmospheric O2 and photosynthetic activity of plants. While performing this work, a variation in pH from neutral to alkaline was observed that may reveal the pathway of elimination of heavy metals through accumulation of metals in rhizospheres and sorption using roots and partly by precipitation. While treating storm wastewater for heavy metal removal, Khan et al. (2009) observed that the optimum pH was 7 and above. Abid et al. (2015) carried out phytoremediation of heavy
TE D
metals by plants and observed the optimum heavy metal removal efficiency in the alkaline pH range.
3.3. Relation of retention time and heavy metal removal
EP
The relation of retention time and heavy metal removal was studied using Spearman rank order correlation. For the three cultivated experimental phases of S1-S4, significant and negative correlation coefficients of Fe,
AC C
Ni, Cu, Zn, Cr, Pb, Mg and Cd levels with retention period were determined that ensured the positive relation of retention period and Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd removal percentages at p<0.05 (Table 3). Babu et al. (2015) studied similar significant correlations for bioremediation of heavy metal-contaminated soil using Miscanthus sinensis. The Fe removal tendency from S1-S4 wastewater using Typha angustifolia sp. and Limnocharis flava sp. and
their combination is revealed in Figure 3. A gradual decline in Fe levels with a retention period of 13 days can be observed in Figure 3. An identical removal tendency was observed for other metals, including Ni, Cu, Zn, Cr, Pb, Mg and Cd. Gala et al. (2015) observed a similar decreasing tendency of heavy metals as the
8
ACCEPTED MANUSCRIPT
retention period was increased. The gradual metal absorption of the plants may be the reason for metal removal from wastewater.
RI PT
3.4. Sorption of heavy metals in plants Metal sorption for Fe, Ni, Cu, Cr, Pb, Mg and Cd was greater in Limnocharis flava sp. compared with Typha angustifolia sp., although this was not true for Zn. Mass balance calculations for the highly contaminated sample (S4) are listed in Table 4. The values in Table 4 indicate that elimination of the above-mentioned
SC
heavy metals was equivalent to their net sorption in plants and precipitation. Precipitation occurs due to the oxidation of compounds with the availability of dissolved oxygen. The declining tendency of net accumulation (mg) of heavy metals in the 15 plants studied for the retention period of 13 days was observed
M AN U
as follows: Fe (71)> Zn (50.5)> Mg (10.7)> Cu (9.6)> Cr (6.51)> Pb (6.2)> Ni (4.3)> Cd (3.6) when Typha angustifolia sp. and Limnocharis flava sp. were cultivated together; Fe (70.3)> Zn (48.7)> Mg (8.2)> Cu (8.6)> Cr (5.41)> Pb (5.4)> Ni (3.4)> Cd (2.8) when Limnocharis flava sp. was cultivated alone; and Fe (67.3)> Zn (49.7)> Mg (8.1)> Cu (7.6)> Cr (4.51)> Pb (6.4)> Ni (2.9)> Cd (2.3) when Typha angustifolia sp. was cultivated alone. The outcomes clearly exposed the greater sorption capacity of Limnocharis flava
TE D
sp. for all heavy metals except Zn and Pb. Moreover, an obvious improvement in the sorption capability was observed when both plants were employed together. This may be because of the improvement in the uptake performance of the plants. Lee et al. (2014) employed Brassica juncea, Brassica campestris, Sorghum
EP
bicolor, and Helianthus annuus for the removal of Cu, Zn, Cd, and Ni from contaminated soil and observed Cu, Zn, Cd, and Ni accumulations of 14.87 ± 5.1 mg, 11.75 ± 4.3 mg, 49.19 ± 1.2 mg and 4.39 ± 0.5 mg,
AC C
respectively, in plants. While treating mine drain-contaminated soil for the removal of Fe and Al by Phragmites australis, Guo et al. (2014) observed Fe and Al accumulation of 38.46 ± 1.09 mg g-1 and
0.43 ± 0.06 mg g-1 in plants. While removing heavy metals from aqueous solutions with sunflower, potato,
canola and walnut shell residues, Feizi and Jalali (2015) found that the residues had a metal sorption capacity for Fe of up to 40.9 mg g-1 and for Zn of up to 43.2 mg g-1, both of which are lower than our findings. Furthermore, Khokhar et al., 2015 carried out an experiment to remove heavy metal ions with chemically treated Melia azedarach L. 2 leaves and reported that the maximum sorption capacity for Fe (III) by NaOH-treated bio-sorbent was 38.46 mg g-1, while our finding for Fe was 71 mg g-1.
9
ACCEPTED MANUSCRIPT
3.5 SEM study Figure 4 demonstrates the surface features of heavy metal (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd) sorption at a
RI PT
magnification of 100 and 500. The substance has a porous texture with an enormous, reachable surface area that supports metal absorption. The surface of the biomass and pores represent the absorption of heavy
SC
metals (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd).
4. Conclusions
The concrete results of this study revealed that the integrated phytogreen system consisting of two different
M AN U
aquatic plants, namely, Typha angustifolia sp. and Limnocharis flava sp. in a conventional oxidation pond process is a reliable and ecologically attractive option. In particular, maximal heavy metal removal (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd) was realized when Typha angustifolia sp. and Limnocharis flava sp. were cultivated together for a retention time of 13 days. Metal removal efficiency was increased when the combined culture of the two plants was employed in comparison with monoculture, and Limnocharis flava
TE D
sp. showed better performance than Typha angustifolia sp. A positive relation between retention time and heavy metal removal was studied and confirmed by the negative and significant correlation coefficients of the corresponding heavy metals (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd) with retention period. The elimination
EP
of the above-mentioned heavy metals was equivalent to their net sorption in plants due to natural precipitation Limnocharis flava sp. showed greater sorption capability than Typha angustifolia sp. for all
AC C
tested heavy metals except Zn and Pb. The scientific contribution of this integrated phytogreen system consisting of two different aquatic plants, namely, Typha angustifolia sp. and Limnocharis flava sp. in the
conventional oxidation pond process may play a role in solving the urgent environmental issues of emission mitigation of heavy metal contamination management. All of the plants used are available free of cost,
making their implementation as absorbents of heavy metals an economically attractive alternative in the
wastewater treatment process. The industrial application of this green technology may make the heavy metal removal process more cost effective.
10
ACCEPTED MANUSCRIPT
Acknowledgements
RI PT
The authors are grateful to the Universiti Malaysia Pahang (UMP), the Faculty of Civil Engineering and Earth Resources (FKASA), Majlis Bandaran Johor Bahru (MBJB), Ranhill Water Services (RWS), Ranhill Utilities Berhad (RUB) and the Danish International Development Agency (DANIDA) for their support. This contemporary investigation was made possible by a grant from the Ministry of Education (MOE)
SC
Malaysia; Fundamental Research Grant Scheme (FRGS) – Vote no: RDU 070108, UMP PreCommercialization Grant – Vote no. UIC 090302 and Prototype Research Grant Scheme (PRGS) – Vote no:
M AN U
RDU120806).
References
TE D
Abhilash, P.C., Pandey, V. C., Srivastava, P., Rakesh, P.S., Chandran, S., Singh, N., Thomas, A.P., 2009. Phytofiltration of cadmium from water by Limnocharis flava (L.) Buchenau grown in freefloating culture system. J. Hazard. Mater. 170, 791–797.
EP
Abid, U., Sun, H., Muhammad, F. H. M., Shah, F., Xiyan, Y., 2015. Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: A review. Environ. Exp. bot. 117, 28-40.
AC C
Ahmadi, A., Heidarzadeh, S., Mokhtari, A. R., Darezereshki, E., Harouni H. A., 2014. Optimization of heavy metal removal from aqueous solutions by maghemite (γ-Fe2O3) nanoparticles using response surface methodology. J. Geochem. Explor. 147, 151-158. Akcil, A., Erust, C., Ozdemiroglu, S., Fonti, V., Beolchini, F., 2015. A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J. Clean. Prod. 86, 24-36. APHA, 2005. Standard methods for the examination of water and wastewater, 20 th ed. Am Public Health Association, Maryland, USA.
11
ACCEPTED MANUSCRIPT
Babu, A. G., Shea, P. J., Sudhakar, D., Jung, I. B., Oh, B. T., 2015. Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal (loid)-contaminated mining site soil. J. Environ. Manage. 151, 160-166.
RI PT
Bah, A. M., Sun, H., Chen, F., Zhou, J., Dai, H., Zhang, G., Wu, F., 2010. Comparative proteomic analysis of Typha angustifolia leaf under chromium, cadmium and lead stress. J. Hazard. Mater. 184, 191–203.
Byungryul, A., Chang, L., Mi-Kyung, S., Jae-Chun, R., Soonjae, L., Seong-Jik, P., Dongye, Z., Song-
SC
Bae, K., Chanhyuk, P., Sang-Hyup, L., Seok, W. H., Jae-Woo, C., 2015. Applicability and toxicity evaluation of an adsorbent based on jujube for the removal of toxic heavy metals. Rea. Func. Pol. 93,
M AN U
138-147.
Cegłowski, M., Schroeder, G., 2015. Preparation of porous resin with Schiff base chelating groups for removal of heavy metal ions from aqueous solutions. Chem. Eng. J. 263, 402-411. Chandra, R., Yadav, S., 2010. Potential of Typha angustifolia for phytoremediation of heavy metals from aqueous solution of phenol and melanoidin. Ecol. Eng. 36, 1277–1284. Deng, G., Li, M., Li, H., Yin, L., Li, W., 2014. Exposure to cadmium causes declines in growth and
TE D
photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). Aquat. Bot. 112, 23-32. Fassett, N.C., Calhoun, B. 1952. Introgression between Typha latifolia and T. angustifolia. Evolution 6, 267-379.
EP
Feizi, M. and Jalali, M., 2015. Removal of heavy metals from aqueous solutions using sunflower, potato, canola and walnut shell residues. J. Taiwan. Inst. Chem. E. 00, 1–12.
AC C
Galal, T. M., Hanaa, S. Shehata, H. S., 2015. Bioaccumulation and translocation of heavy metals by Plantago major L. grown in contaminated soils under the effect of traffic pollution. Ecol. Indic. 48, 244-251.
González, A. G., Cuadros, F., Celma, A. R., Rodríguez, F. L., 2014. Influence of heavy metals in the biomethanation of slaughterhouse waste. J. Clean. Prod. 65, 473-478. Gopal, B., Sharma, K.P. 1980. Aquatic weed control versus utilization. Econ. Bot. 33, 340-346. Grace, J.B., Wetzel, R.G. 1981. Effects of size and growth rate on vegetative reproduction in Typha. Oecologia 50, 158-161.
12
ACCEPTED MANUSCRIPT
Guo, L., Ott, D. W., Cutright, T. J., 2014. Accumulation and histological location of heavy metals in Phragmites australis grown in acid mine drainage contaminated soil with or without citric acid. Environ. Exp. Bot. 105, 46-54.
RI PT
Gustafson, T.D. 1976. Production, photosynthesis and the storage and utilization of reserves in a natural stand of Typha latifolia L. PhD thesis. University of Wisconsin-Madison, 102.
Han, Y., Hwang, G., Kim, D., Park, S., Kim, H., 2015. Porous Ca-based bead sorbents for simultaneous removal of SO2, fine particulate matters, and heavy metals from pilot plant sewage sludge
SC
incineration. J. Hazard. Mater. 283, 44-52.
Hu, Y., Wang, D., Wei, L., Zhang, X., Song, B., 2014. Bioaccumulation of heavy metals in plant leaves
M AN U
from Yan׳an city of the Loess Plateau, China. Ecotox. Environ. Safe. 110, 82-88. Khan, E., Khaodhir, S., Ruangrote, D., 2009. Effects of moisture content and initial pH in composting process on heavy metal removal characteristics of grass clipping compost used for storm water filtration. Bioresour. Technol. 100, 4454-4461.
Khokhar, A., Siddique, Z., Misbah, 2015. Removal of heavy metal ions by chemically treated Melia azedarach L. 2 leaves. J. Environ. Chem. Eng. doi:10.1016/j.jece.2015.03.009.
TE D
Ladislas, S., Gérente, C., Chazarenc, F., Brisson, J., Andrès, Y., 2014. Floating treatment wetlands for heavy metal removal in highway stormwater ponds. Ecol. Eng. doi:10.1016/j.ecoleng.2014.09.115. Lara, M. A. M., Blázquez, G., Trujillo, M.C., Pérez, A., Calero, M., 2014. New treatment of real
EP
electroplating wastewater containing heavy metal ions by adsorption onto olive stone. J. Clean. Prod. 81, 120-129.
AC C
Lee, J., Sung, K., 2014. Effects of chelates on soil microbial properties, plant growth and heavy metal accumulation in plants. Ecol. Eng. 73, 386-394. Liu, W. J., Zeng, F. X., Jiang, H., Zhang, X. S., 2011. Adsorption of lead (Pb) from aqueous solution with Typha angustifolia biomass modified by SOCl2 activated EDTA. Chem. Eng. J. 170, 21–28. Marchand, L., Nsanganwimana, F., Oustrière, N., Grebenshchykova, Z., Allende, K. L., Mench, M., 2014. Copper removal from wastewater using a bio-rack system either unplanted or planted with Phragmitesaustralis, Juncus articulates and Phalaris arundinacea. Ecol. Eng. 64, 291–300.
13
ACCEPTED MANUSCRIPT
Matouq, M., Jildeh, N., Qtaishat, M., Hindiyeh, M., Syouf, M.Q.A., 2015. The adsorption kinetics and modeling for heavy metals removal from wastewater by Moringa pods. J. Environ. Chem. Eng. 3, 775784.
RI PT
Mendoza, R. E., García, I. V., Cabo, L. D., Weigandt, C. F., Iorio, A. F. D., 2015. The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River Basin (Argentina). Sci. Total Environ. 505, 555-564.
Mesa, J., Naranjo, E. M., Caviedes, M.A., Gómez, S. R., Pajuelo, E., Llorente, I. D. R., 2015. Scouting
SC
contaminated estuaries: Heavy metal resistant and plant growth promoting rhizobacteria in the native metal rhizoaccumulator Spartina maritima. Mar. Pollut. Bull. 90, 150-159.
M AN U
Mohammad, I. A., Adel, R. A. Usman, Ahmed, H. E., Anwar, A. A., Hesham, M. I., Salem, E., Abdulrasoul, A., 2015. Conocarpus biochar as a soil amendment for reducing heavy metal availability and uptake by maizeplants. Saudi. J. biol. sci. 22, 503-511.
Morteza, F., Mohsen, J., 2015. Removal of heavy metals from aqueous solutions using sunflower,
Nguyen,
canola and walnut shell residues. J. Taiwan Inst. Chem. E. doi:10.1016/j.jtice.2015.03.027.
V.
TE D
potato,
K.,
Lee,
J.U.,
2015.
Effect of sulfur
concentration on microbial
removal of arsenic and heavy metals from mine tailings using mixed culture of Acidithiobacillus spp. J. Geochem. Explor. 148, 241-248.
EP
Oosten, M. J. V., Maggio, A., 2015. Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ. Exp. Bot. 111, 135-146.
AC C
Philippe, A. G., Masotti, V., Höhener, P., Boudenne, J. L., Viglione, J., Schwob, I. L., 2014. Constructed wetlands to reduce metal pollution from industrial catchments in aquatic Mediterranean ecosystems: A review to overcome obstacles and suggest potential solutions. Environ. Int. 64, 1-16. Ponce, S. C., Prado, C., Pagano, E., Prado, F. E., Rosa, M., 2015. Effect of solution pH on the dynamic
of biosorption of Cr (VI) by living plants of Salvinia minima. Ecol. Eng. 74, 33-41. Pratas, J., Paulo, C., Favas, P. J. C., Venkatachalam, P., 2014. Potential of aquatic plants for phytofiltration of uranium-contaminated waters in laboratory conditions. Ecol. Eng. 69, 170-176.
14
ACCEPTED MANUSCRIPT
Rezania, S., Ponraj, M., Talaiekhozani, A., Mohamad, S. E., Din, M. F. M., Taib, S. M., Sabbagh, F., Sairan, F. M. 2015. Perspectives of phytoremediation using water hyacinth for removal of heavy metals, organic and inorganic pollutants in wastewater. J. Environ. Manage. 163, 125-133.
RI PT
Rodolfo, E. M., Ileana, V. G., Laura, D. C., Cristian, F. W., Alicia, F. D. I., 2015. The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River Basin (Argentina). Sci. total. environ. 505, 555-564.
Said, M., Cassayre, L., Dirion, J. L., Nzihou, A., Joulia, X. 2015. Behavior of heavy metals during
SC
gasification of phytoextraction plants: thermochemical modelling. Compu. Aid. Chem. Eng. 37, 341346.
M AN U
Sargın, İ., Kaya, M., Arslan, G., Baran, T., Ceter, T., 2015. Preparation and characterisation of biodegradable pollen–chitosan microcapsules and its application in heavy metal removal. Bioresour. Technol. 177, 1-7.
Shavandi, M.A., Haddadian, Z., Ismail, M.H.S., Abdullah, N., Abidin, Z.Z., 2012. Removal of Fe (III), Mn(II) and Zn(II) from palm oil mill effluent (POME) by natural zeolite. J. Taiwan Inst. Chem. E. 43, 750-759.
TE D
Siddique, M.N. I., Munaim, M.S.A, Zularisam, A.W., 2014. Feasibility analysis of anaerobic codigestion of activated manure and petrochemical wastewater in Kuantan (Malaysia). J. Clean. Prod., In Press, Accepted Manuscript, Available online 19 August 2014, doi:10.1016/j.jclepro.2014.08.003.
EP
Smain, M., Saida, S., Michel, C., 2009. Toxicity and removal of heavy metals (cadmium, copper, and zinc) by Lemna gibba. Ecotox. Environ. Safe. 72, 1774-1780.
AC C
Smith, S.G., 1962. Natural hybridization among five species of cattail. Am. J. Bot. 49, 678. Syukor, A.R., Zularisam, A.W., Zakaria, I., Ismid, M., Sulaiman, S., Halim, A., Thomas, D. L., 2013. Potential of Aquatic Plant as Phytoremediator for Treatment of Petrochemical Wastewater in Gebeng Area, Kuantan. Adv. Environ. Biol. 7, 3808–3814. Syukor, A.R., Zularisam, A.W., Ideris, Z., Ismid, M.S. M., Nakmal, H.M., Sulaiman, S., Hasmanie, A.H., Norsita, M.R.S., Nasrullah, M., 2014. Performance of Phytogreen Zone for BOD5 and SS Removal for Refurbishment Conventional Oxidation Pond in an Integrated Phytogreen System. Int. J. Environ. Ear. Sci. Eng. 8, 164-169.
15
ACCEPTED MANUSCRIPT
Taylor, Crowder, 1984. Cooper and Nickel tolerance in T. latifolia clones from contaminated and uncon. envir. Can J. Bot. 62, 1304-1308. Wilcox, D.A., Apfelbaum, S.I., R. Hiebert. 1984. Cattail invasion of sedge meadows following
Soc. of Wetlands Scientists 4, 115-128.
RI PT
hydrologic disturbance in the Cowles Bog Wetland Complex, Indiana Dunes National Lakeshore. J.
Xu, W., Shi, W., Yan, F., Zhang, B., Liang, J., 2011. Mechanisms of cadmium detoxification in cattail (Typha angustifolia L.). Aquat. Bot. 94, 37–43.
SC
Zhu, C., Tian, H., Cheng, K., Liu, K., Wang, K., Hua, S., Gao, J., Zhou, J., 2015. Potentials of whole process control of heavy metals emissions from coal-fired power plants in China. J. Clean. Prod., in
AC C
EP
TE D
M AN U
Press, Corrected Proof, Available online 21 May 2015, doi:10.1016/j.jclepro.2015.05.008.
16
ACCEPTED MANUSCRIPT
Characteristics of wastewater obtained from four stations (S1- S4) S3
S4
847±0.9 292±0.64 1.86±0.05 7.79±0.01 30.8±0.15 0.45±0.001 14±0.02 17±0.01 0.23±0.002 0.05±0.001 0.35±0.002 0.3±0.002 0.32±0.002 0.16±0.001 0.22±0.002 0.3±0.002
848±1 293±0.7 1.87±0.06 7.8±0.01 30. 85±0.28 0.46±0.001 15±0.02 18±0.01 0.24±0.002 0.06±0.001 0.4±0.003 0.35±0.003 0.38±0.003 0.17±0.001 0.23±0.002 0.29±0.002
846±0.9 291±0.6 1.85±0.05 7.78±0.01 29.9±0.17 0.44±0.001 13±0.01 16±0.01 0.22±0.001 0.04±0.001 0.29±0.001 0.24±0.001 0.27±0.001 0.15±0.001 0.21±0.001 0.28±0.001
845±0.8 290±0.53 1.84±0.04 7.77±0.01 29.4±0.14 0.43±0.001 12±0.01 15±0.01 0.21±0.001 0.03±0.001 0.2±0.001 0.20±.001 0.250±.001 0.14±0.001 0.2±0.001 0.27±0.001
EP
TE D
M AN U
S2
AC C
COD (mgL-1) BOD (mgL-1) DO (mgL-1) pH Temperature (ºC) Conductivity (mScm-1) Nitrate (mgL-1) Phosphorous (mgL-1) Pb (mgL-1) Cd (mgL-1) Cr (mgL-1) Cu (mgL-1) Mg (mgL-1) Ni (mgL-1) Zn (mgL-1) Fe (mgL-1)
S1
SC
Table1
RI PT
List of Tables
Values are the mean + S.E. of the 4 replicates
1
ACCEPTED MANUSCRIPT
Table2
Heavy metals (%)
Plant mean
S2
S3
S4
Lim
56.3±0.2a 55.3±0.2a 54.6±0.3a 53.7±0.2a 49.5±0.2a 45.2±0.3a 44.2±0.3a 43.3±0.3a
57.7±0.2b 56.7±0.2b 57.4±0.3b 57.1±0.2b 52.3±0.2b 47.2±0.3b 46.2±0.3b 46.4±0.3b
61.2±0.2c 60.2±0.2c 60.3±0.3c 59.2±0.2c 55.4±0.3c 51.5±0.3c 50.5±0.3c 46.7±0.3c
62.4±0.2d 61.4±0.2d 63.4±0.3d 60.5±0.2d 57.5±0.2d 52.4±0.3b 51.4±0.3b 48.5±0.3d
57.6±0.2b 56.6±0.2b 58.2±0.2b 56.2±0.2b 52.4±0.2b 46.3±0.2b 45.3±0.2b 44.4±0.3b
Typ
Lim+ Typ
53.7±0.2a 52.7±0.2a 52.3±0.2a 53.4±0.2a 46.5±0.2a 41.1±0.2a 40.1±0.2a 40.5±0.3a
63.2±0.2c 62.2±0.2c 61.8±0.2c 59.6±0.2c 58.3±0.2c 54.7±0.2c 53.7±0.2c 49.3±0.3c
SC
S1
M AN U
Fe Ni Cu Zn Cr Pb Mg Cd
Station mean
RI PT
Assessment of heavy metal removal efficiency between stations and plants
AC C
EP
TE D
The values followed by same letter are not significantly different at the 0.05 probability level. Lim = Limnocharis flava sp. and Typ = Typha angustifolia sp.
2
ACCEPTED MANUSCRIPT
Table 3 The relationship between retention time and heavy metal removal at p<0.05
Zn
Cr
Pb
Mg
Cd
Correlation coefficient S4
Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ
-0.84 -0.90 -0.91 -0.94 -0.92 -0.93 -0.93 -0.91 -0.94 -0.93 -0.90 -0.97 -0.97 -0.90 -0.89 -0.98 -0.95 -0.87 -0.94 -0.92 -0.95 -0.89 -0.95 -0.92
-0.98 -0.94 -0.91 -0.92 -0.98 -0.93 -0.96 -0.94 -0.96 -0.87 -0.93 -0.92 -0.90 -0.92 -0.86 -0.97 -0.96 -0.97 -0.97 -0.95 -0.97 -0.86 -0.84 -0.88
-0.91 -0.88 -0.97 -0.80 -0.96 -0.94 -0.93 -0.87 -0.89 -0.92 -0.98 -0.95 -0.80 -0.95 -0.88 -0.92 -0.84 -0.94 -0.94 -0.88 -0.90 -0.93 -0.36 -0.96
-0.87 -0.90 -0.92 -0.91 -0.92 -0.94 -0.84 -0.89 -0.89 -0.98 -0.88 -0.90 -0.99 -0.99 -0.95 -0.92 -0.93 -0.94 -0.85 -0.90 -0.90 -0.86 -0.87 -0.96
SC
RI PT
Correlation coefficient S3
M AN U
Cu
Correlation coefficient S2
TE D
Ni
Correlation coefficient S1
EP
Fe
Plants
AC C
Heavy metals
3
ACCEPTED MANUSCRIPT
Table 4 Mass Balance calculations of heavy metals in Limnocharis flava sp., Typha angustifolia sp. and their combination (retention period 13 days)
Zn
Cr
Pb
Mg
Cd
R (mg)
Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ
7.3±0.23 7.3±0.23 7.3±0.23 4.46±0.08 4.46±0.08 4.46±0.08 5.54±0.15 5.54±0.15 5.54±0.15 6.09±0.24 6.09±0.24 6.09±0.24 7.14±0.08 7.14±0.08 7.14±0.08 3.04±0.08 3.04±0.08 3.04±0.08 5.57±0.15 5.57±0.15 5.57±0.15 3.99±0.12 3.99±0.12 3.99±0.12
1.46±0.07 2.04±0.17 2.49±0.16 1.18±0.05 1.48±0.1 1.73±0.09 1.29±0.17 1.74±0.18 1.86±0.17 1.5±0.14 1.83±0.15 1.71±0.08 2.27±0.18 2.57±0.08 3.09±0.07 0.98±0.08 1.12±0.1 1.42±0.08 1.3±0.17 1.76±0.18 1.86±0.17 1.59±0.13 1.69±0.23 2.02±0.13
4.29±0.15 3.71±0.16 3.26±0.21 2.55±0.09 2.25±0.09 2±0.08 2.52±0.38 2.07±0.37 1.95±0.36 3.49±0.39 3.16±0.49 3.28±0.37 3.79±0.17 3.49±0.07 2.97±0.08 1.63±0.09 1.49±0.17 1.19±0.1 2.53±0.38 2.07±0.37 1.97±0.36 1.75±0.04 1.65±0.33 1.32±0.33
1.55±0.09 1.55±0.09 1.55±0.09 0.73±0.08 0.73±0.08 0.73±0.08 1.73±0.08 1.73±0.08 1.73±0.08 1.1±0.18 1.1±0.18 1.1±0.18 1.08±0.11 1.08±0.11 1.08±0.11 0.43±0.08 0.43±0.08 0.43±0.08 1.74±0.08 1.74±0.08 1.74±0.08 0.65±0.28 0.65±0.28 0.65±0.28
SC
RI PT
Net amount absorbed by plants (mg)
M AN U
Cu
Effluent concentration (mg)
TE D
Ni
Influent concentration (mg)
EP
Fe
Plants
AC C
Heavy metals
Values are the mean + S.E. of the 4 observations, Lim = Limnocharis flava sp. and Typ = Typha angustifolia sp.R=Heavy metal removal by natural degradation in control
4
ACCEPTED MANUSCRIPT
M AN U
SC
RI PT
List of Figures
AC C
EP
TE D
Fig. 1. Layout of experimental set up, where influent zone (Z1), Phytogreen zone (Z2), Aeration zone (Z3), Inclined Plate Clarifier zone (Z4) and effluent zone (Z5); S1-S15 in-situ sampling points.
1
AC C
EP
TE D
Fig. 2. Photograph of experimental set up.
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
2
ACCEPTED MANUSCRIPT
SC
RI PT
Fe removal from station 1 (S1) wastewater
M AN U
a
AC C
b
EP
TE D
Fe removal from station 2 (S2) wastewater
3
ACCEPTED MANUSCRIPT
SC
RI PT
Fe removal from station 3 (S3) wastewater
M AN U
c
AC C
d
EP
TE D
Fe removal from station 4 (S4) wastewater
Fig. 3. (a-d) Effect of Typha angustifolia sp., Limnocharis flava sp. and their combination on Fe concentrations of S1 to S4 wastewater , where Typ = Typha angustifolia sp, Lim = Limnocharis flava sp.
4
ACCEPTED MANUSCRIPT
a
M AN U
SC
RI PT
b
d
AC C
EP
TE D
c
Fig. 4. SEM of (a, c) heavy metals loaded dried (Thypha angustifolia) biomass (b, d) heavy metals loaded dried (Limnocharis flava) biomass ×100 and 500.
5
ACCEPTED MANUSCRIPT
Highlights
The combination of Limnocharis flava and Typha angustifolia improved heavy metal removal.
RI PT
•
A longer retention period improved Heavy metal removal.
•
The removal of heavy metals was equivalent to their net sorption in plants
•
Limnocharis flava sp. exhibited greater metal sorption capacities
AC C
EP
TE D
M AN U
SC
•
S0959-6526(15)01575-9
DOI:
10.1016/j.jclepro.2015.10.103
Reference:
JCLP 6334
To appear in:
Journal of Cleaner Production
Received Date: 25 January 2015 Revised Date:
23 October 2015
Accepted Date: 24 October 2015
Please cite this article as: Syukor ARA, Sulaiman S, Siddique MNI, Zularisam AW, Said MIM, Integration of Phytogreen for heavy metal removal from wastewater, Journal of Cleaner Production (2015), doi: 10.1016/j.jclepro.2015.10.103. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
b
M AN U
SC
RI PT
a
d
EP
TE D
c
Fig. SEM of (a, c) heavy metals loaded dried (Thypha angustifolia) biomass (b, d) heavy metals loaded
AC C
dried (Limnocharis flava) biomass ×100 and 500.
The Graphical Abstract.
1
ACCEPTED MANUSCRIPT
Integration of Phytogreen for heavy metal removal from wastewater
*
E-mail: [email protected]
RI PT
A.R. Abdul Syukora*, S. Sulaimana, Md. Nurul Islam Siddiqueb, A. W. Zularisamb, M.I.M. Saidc
Tel: +60 9 5492931; Fax: +60 9 5492998 a
Faculty of Civil Engineering and Earth Resources, University Malaysia Pahang (UMP), Lebuhraya Tun
b
SC
Razak, 26300 Gambang, Kuantan, Pahang, Malaysia.
Faculty of Engineering Technology, University Malaysia Pahang (UMP), Lebuhraya Tun Razak, 26300
c
M AN U
Gambang, Kuantan, Pahang, Malaysia.
Faculty of Civil Engineering, Universiti Teknologi Malaysia (UTM), 81310 University Technology Malaysia Skudai, Johor, Malaysia.
Abstract
TE D
Although the oxidation pond process for the treatment of wastewater has been widely studied and commercial application has already been recognized, the integration of the phytogreen system has yet to be studied. This work was focused on investigating the improvement in the conventional oxidation pond process produced by the integrated phytogreen system for the treatment of wastewater. Among the
EP
conventional treatment systems, the phytogreen integrated oxidation pond process appears to be an efficient system, affecting the bio-removal of heavy metals. The influence of the integrated Phytogreen system,
AC C
including two different aquatic plants (Typha angustifolia sp. and Limnocharis flava sp.) in the conventional oxidation pond process, was investigated for a retention time of 13 days. The results revealed that the integrated Phytogreen system realized the maximum removal of copper to 79.07%, magnesium to 68%, cadmium to 61.07%, chromium to 69.17%, nickel to74.87%, iron to 81.17%, lead to 62.07% and zinc to 63% at a retention time of 13 days when the two plant species were combined together. A positive relation between retention time and heavy metal removal was studied, and it was confirmed by the negative and significant correlation coefficients of the corresponding heavy metals with retention period. The results revealed that the integrated phytogreen system consisting of two different aquatic plants (Typha angustifolia
1
ACCEPTED MANUSCRIPT
sp. and Limnocharis flava sp.) in the conventional oxidation pond process is a reliable and ecologically attractive option. Finally, integration of Phytogreen is proposed to minimize heavy metal contamination in wastewater.
RI PT
Keywords: Retention time, wastewater, Phytogreen, heavy metal removal.
1. Introduction
A range of commercial activities such as mining, plating, dyeing, automobile manufacturing and metal
SC
processing are responsible for heavy metal contamination of our environment (Matouq et al., 2015). This contamination has introduced numerous environmental problems (Zhu et al., 2015). The proper monitoring
M AN U
of heavy metals in wastewater is obligatory for maintaining water and food quality standards (Han et al., 2015).
Protection of the environment is one of the key concerns of this century (Smain et al., 2009). In particular, the discharge of natural or synthetic materials is one of the most substantial factors contributing to the degradation of the biosphere (Siddique et al., 2014). Aquatic environments are the end destinations of these substances, and they frequently carry high concentrations of pollutants that may be toxic for organisms
TE D
(Rodolfo et al., 2015). Among these polluting substances, heavy metals are easily transported and accumulated in the environment (Byungryul et al., 2015). They reach aquatic environments as dissolved and solid waste from domestic, industrial, and agricultural runoffs (Smain et al., 2009).
EP
The discharge of inadequately treated municipal sewage and industrial waste containing heavy metals into waterways has become a severe environmental issue for the civilization (Siddique et al., 2014). The use of
AC C
heavy metal-contaminated water poses a hazard to public health (Akcil et al., 2015). Removal of heavy metals by conventional chemical treatment methods such as precipitation, coagulation–flocculation, adsorption, ion exchange, membrane filtration and other advanced oxidation processes involves huge operational and supervision costs (Lara et al., 2014). Therefore, it has become obligatory to recommend a cost-effective green technology to eliminate these heavy metals and improve the effluent standard (González et al., 2014). Integration of Phytogreen in heavy metal removal from wastewater has numerous advantages. Aquatic plants are able to act as natural absorbers of heavy metals and other contaminants (Pratas et al., 2014).
2
ACCEPTED MANUSCRIPT
Elimination of heavy metals and other contaminants from wastewater by aquatic plants has been recommended as the most economic and efficient method (Philippe et al., 2014). In the past few decades, aquatic plants or fabricated wetlands were applied widely for the elimination of heavy metals and
RI PT
contaminants from wastewater (Mesa et al., 2015). Among aquatic plants, emergent plants are capable of accumulating metals in their tissues over several times the concentration of that in the adjacent environment, which may be caused by metal uptake of the plants through adsorption to anionic sites in the cell walls (Deng et al., 2014). However, integration of Phytogreen technology in heavy metal removal from
SC
wastewater is time consuming (Syukor et al., 2013). The cultivation and growth of the aquatic plants usually takes a significant amount time, which may be a disadvantage of this technology (Said et al., 2015).
M AN U
However, the disadvantages of this green technology can be offset by its numerous advantages (Syukor et al., 2014).
Typha angustifolia sp. and Limnocharis flava sp. are recognized hyper-accumulator emergent plants (Rezania et al., 2015). These plants grow in marshlands and sedge meadows and along slow-moving streams, river banks, and lake shores. These two plants are found in regions of fluctuating water levels such
TE D
as roadside ditches, reservoirs and other disturbed wet soil areas. Typha angustifolia sp. is usually limited to unstable surroundings, habitually with basic, calcareous, or somewhat salty soils (Fassett and Calhoun 1952). Cattail can grow in deep water compared with Typha angustifolia sp., although both plants can
EP
achieve maximum growth at a water depth of 50 cm (20 inches) (Grace and Wetzel 1981). The tolerance of Typha angustifolia sp. to high concentrations of lead, zinc, copper, and nickel has been established (Taylor
AC C
and Crowder 1984). This species has been used in secondary wastewater treatment schemes (Gopal and Sharma 1980) and has been observed in most suitable sites where it contests against other species. Typha angustifolia sp. and Typha domingensis sp. are limited to less favorable and more saline environments when they grow with Typha latifolia sp. (Gustafson 1976). Typha latifolia sp.
often replaces Typha angustifolia
sp. in shallow (\<15 cm) depths, limiting the other species to deep water (Grace and Wetzel 1981). Typha
angustifolia sp. is believed to be a pioneer species for secondary succession of disturbed bogs (Wilcox et al. 1984). Apparently, an incremental change in the acidity of a bog decreases both the pH and the incursion of Typha angustifolia sp. According to Theodore Cochran (pers. comm.) of the University of Wisconsin-
3
ACCEPTED MANUSCRIPT
Madison herbarium, most early herbarium specimens are Typha latifolia sp., and only recently have Typha angustifolia sp. been collected from Wisconsin wetlands. In 1962, Smith was the first to report on the heavy metal removal efficiency of these plants. These two plants can accumulate heavy metals such as copper,
RI PT
cadmium, chromium, nickel and lead at levels of up to 0.1% and iron and zinc at levels of up to 1% of the plant dry weight (Ponce et al., 2015). Several studies have been carried out on the metal removal performance of these two plants (Chandra and Yadav in 2010; Bah et al., in 2010; Xu et al., in 2011; Liu et al., in 2011 and Abhilash et al., in 2009). However, these particular plants are not being used for heavy
SC
metal elimination commercially. There is still a huge scarcity of data confirming the contributions of Typha angustifolia and Limnocharis flava when cultivated together for the elimination of heavy metals. Although
M AN U
the oxidation pond process for the treatment of wastewater has been widely studied and commercial application has already been recognized, the integration of the phytogreen system has yet to be studied. Consequently, this manuscript may help meet the increasing demand of society for heavy metal removal. Therefore, the key objectives of the present study were to determine the heavy metal removal efficiency of the integrated Phytogreen system consisting of two different aquatic plants, namely, Typha angustifolia sp. and Limnocharis flava sp., in the conventional oxidation pond process and the relationship between the
TE D
retention time and heavy metal removal.
2. Materials and Methods
EP
Raw municipal sewage and industrial wastewater were obtained from four sampling stations (S1-S4) along the 12 km of Karteh, Malaysia (6° 5' 59N, 100° 21' 6E) and transported to the laboratory for experimental
AC C
use. To minimize error during sampling, each sample was obtained separately and used as four discrete replicates.
Batch tests were carried out with similar samples obtained during similar phases.
Characterization of the obtained samples is shown in Table 1. Typha angustifolia and Limnocharis flava
were collected from the Gebeng industrial area and Pekan of Malaysia.
2.1. Experimental Setup The integrated phytogreen system consisted of five zones: the influent zone (Z1), the Phytogreen zone (Z2), the aeration zone (Z3), the inclined plate clarifier zone (Z4) and the effluent zone (Z5) (Fig. 1). Each
4
ACCEPTED MANUSCRIPT
phytogreen system zone had a capacity of 75 L and was connected with a 20 PVC pipe that had a diameter of 5 cm and pores with a diameter of 25 mm to ensure fluid exchange. While performing this work, Typha angustifolia sp. and Limnocharis flava sp. plants of 34.4±1.5 cm in length and 44.6±0.4 g in weight were
RI PT
chosen and planted in the phytogreen zone. Phase 1 consisted of only Typha angustifolia sp. at a density of 30 plants per m2. Phase 2 consisted of only Limnocharis flava sp. at a density of 30 plants per m2. During phase 3, both Typha angustifolia sp. and Limnocharis flava sp. were planted at a density of 15 plants per m2. Phase 4 was treated as a control group (without plants) for the determination of heavy metal removal by
SC
nature.
M AN U
2.2. Operational design
Acclimatization of the selected plants was carried out using distilled water for 7 days; the selected plants were cleaned properly with distilled water before being used in the phytogreen zone. Then, 60 L of raw wastewater obtained from the four different stations (S1-S4) was fed to each of the experimental phases and subjected to 10 hours of sunlight. Double-distilled water was used to balance the evaporation loss at a fixed interval; the pH of the wastewater remained fixed, as a small amount of double distilled water was added to
Fig. 1 and Fig. 2.
EP
2.3. Methods
TE D
balance the amount lost. A schematic drawing and photograph of the total experimental setup are shown in
Samples were obtained individually starting from the first to 13th day of treatment from the four individual
AC C
experimental phases: S1-S4. pH, COD, BOD, total nitrogen and P for inflowing and outgoing waste were analyzed using standard procedures (APHA, 2005). The concentrations of heavy metals were analyzed through a scheme of sequential extraction according to the procedure of Nguyen and Lee (2014). ICP-OES was applied to analyze the concentration of heavy metals in the extracted liquor during the sequential extraction processes.
5
ACCEPTED MANUSCRIPT
2.4. Statistical Analysis A Kolmogorov–Smirnov (K–S) test was used to investigate the normality of the obtained data. A 3-way analysis of variance (ANOVA) was carried out to assess the effect of the plants, heavy metal concentrations
RI PT
and retention times on the removal of heavy metals. To determine the differences among the averages, a Duncan multiple range test (alpha = 0.05) was carried out. Correlation between the heavy metal level and retention time was determined by Spearman rank order correlation.
The Spearman rank coefficient is analyzed based on two criteria: (a) the variables should be intervals or
SC
ratios, and (b) a monotonic relationship exists between them. Both criteria were fulfilled; the retention time and heavy metal concentrations were interval variables and monotonic relationship existed between them.
% removal efficiency =
M AN U
The heavy metal removal percentage was obtained using the following equation:
Ci - Cf X 100 Ci
(1)
Where, Ci and Cf are the initial and final heavy metal concentrations.
TE D
3. Results and Discussion
The effect of the plants, pH and retention time on the removal of heavy metals is explained clearly in this section.
EP
3.1. Performance of plants on heavy metal removal To assess the performance of the selected plants in the removal efficiency of heavy metals, Typha
AC C
angustifolia sp. and Limnocharis flava sp. were cultivated separately and together. Analysis of variance and the Duncan multiple range test (p = 0.05) suggested the maximum removal of Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd for combined culture of Typha angustifolia sp. and Limnocharis flava sp. and minimum removal for Typha angustifolia sp. (Table 2). However, the results revealed that the integrated Phytogreen system
realized the maximum removal of Cu to 79.07%, Mg to 68% Cd to 61.07%, Cr to 69.17%, Ni to74.87%, Fe to 81.17%, Pb to 62.07% and Zn to 63% at a retention time of 13 days when two plants were combined together. Identical results for the enhancement of arsenic and heavy metal removal efficiency from wastewater using a combined culture of A. ferrooxidans and A. thiooxidans was found by Nguyen and Lee in
6
ACCEPTED MANUSCRIPT
2015. The current results are also reinforced by Marchand et al. (2014) during treating wastewater by plants. When Typha angustifolia sp. and Limnocharis flava sp. were cultivated separately and together, the heavy metal removal was increased by the metal uptake of the plants. The uptake methods involve precipitation
RI PT
and co-precipitation (Ladislas et al., 2014). Typha angustifolia sp. and Limnocharis flava sp. provided food and an environment suitable for the propagation of microbes through their rhizosphere, which are the key locations for heavy metals immobilization and uptake by these plants (Mendoza et al., 2015). The combined application of Typha angustifolia sp. and Limnocharis flava sp. indicated that the maximum uptake
SC
efficiency was due to the increase in their rhizospheres. Moreover, the enhanced rhizosphere may help to increase the uptake efficiency of the cell. The defecation of phytosiderophores by the plants results in a
performance (Hu et al., 2014).
M AN U
complex with free heavy metal ions that might be considered a secondary cause for the increase in uptake
The favored order for heavy metal removal was Fe> Ni> Cu> Zn> Cr> Pb> Mg> Cd when the combined culture of Typha angustifolia sp. and Limnocharis flava sp. was employed. While performing phytoremediation of contaminated soil, a similar trend of metal uptake was observed by Oosten and Maggio in 2015. This current method was able to achieve greater Cd and Zn removal from S4 wastewater (49.3%
TE D
and 59.6%) than that observed by Ahmadi et al. (2014) while treating aqueous solutions with maghemite nanoparticles (20% and 52%) (Table 2). Similarly, for Cr removal, the present method showed greater removal efficiency from S4 wastewater (58.3%) than those studied by Ceglowski and Schroeder (2015)
EP
while treating aqueous solutions with a porous resin (Table 2). The greater removal of Cd, Zn and Cr may be due to the plants' greater uptake efficiency of metals when compared with the oxidation process and other
AC C
advanced technologies. Sargın et al. (2015), using pollen–chitosan microcapsules, observed lower removal of Cd (26.6%), Cu (40.8%), Ni (16.2%) and Zn (21%) compared with the findings of the present work. Noticeably, the present work achieved greater Fe removal (81.17%) than that of Shavandi et al. (2012) during POME treatment with natural Zeolite. While treating heavy metal contaminated soil with Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis, Babu et al. (2015) found 36% Zn,
40% Pb and 68% Cu removal, which are 27%, 22.07% and 11% less than our findings. Morteza et al. (2015) examined heavy metal removal efficiency from aqueous solutions using sunflower, potato, canola and walnut shell residues and found that the nickel removal efficiency was approximately 55%, while the present
7
ACCEPTED MANUSCRIPT
work achieved a higher nickel removal efficiency of 62.2% when two plants (Typha angustifolia sp. and Limnocharis flava sp.) were applied together. Mohammad et al. (2015) carried out an experiment on the uptake of heavy metals by maize plants and achieved 21.2% Zn and 29% Cu removal, while this work
3.2. Relation of pH and heavy metal removal
RI PT
achieved 38.4% and 32.8% higher removal for Zn and Cu.
The relation between pH and heavy metal removal was studied by measuring pH and heavy metal density
SC
over the course of the experiment. Primarily, the pH of the S4 wastewater was alkaline in nature. Subsequently, variation in the pH from 6.85±0.01 to 7.79±0.01 was observed. This change in pH may be due
M AN U
to the addition of O2 via the disintegration of the atmospheric O2 and photosynthetic activity of plants. While performing this work, a variation in pH from neutral to alkaline was observed that may reveal the pathway of elimination of heavy metals through accumulation of metals in rhizospheres and sorption using roots and partly by precipitation. While treating storm wastewater for heavy metal removal, Khan et al. (2009) observed that the optimum pH was 7 and above. Abid et al. (2015) carried out phytoremediation of heavy
TE D
metals by plants and observed the optimum heavy metal removal efficiency in the alkaline pH range.
3.3. Relation of retention time and heavy metal removal
EP
The relation of retention time and heavy metal removal was studied using Spearman rank order correlation. For the three cultivated experimental phases of S1-S4, significant and negative correlation coefficients of Fe,
AC C
Ni, Cu, Zn, Cr, Pb, Mg and Cd levels with retention period were determined that ensured the positive relation of retention period and Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd removal percentages at p<0.05 (Table 3). Babu et al. (2015) studied similar significant correlations for bioremediation of heavy metal-contaminated soil using Miscanthus sinensis. The Fe removal tendency from S1-S4 wastewater using Typha angustifolia sp. and Limnocharis flava sp. and
their combination is revealed in Figure 3. A gradual decline in Fe levels with a retention period of 13 days can be observed in Figure 3. An identical removal tendency was observed for other metals, including Ni, Cu, Zn, Cr, Pb, Mg and Cd. Gala et al. (2015) observed a similar decreasing tendency of heavy metals as the
8
ACCEPTED MANUSCRIPT
retention period was increased. The gradual metal absorption of the plants may be the reason for metal removal from wastewater.
RI PT
3.4. Sorption of heavy metals in plants Metal sorption for Fe, Ni, Cu, Cr, Pb, Mg and Cd was greater in Limnocharis flava sp. compared with Typha angustifolia sp., although this was not true for Zn. Mass balance calculations for the highly contaminated sample (S4) are listed in Table 4. The values in Table 4 indicate that elimination of the above-mentioned
SC
heavy metals was equivalent to their net sorption in plants and precipitation. Precipitation occurs due to the oxidation of compounds with the availability of dissolved oxygen. The declining tendency of net accumulation (mg) of heavy metals in the 15 plants studied for the retention period of 13 days was observed
M AN U
as follows: Fe (71)> Zn (50.5)> Mg (10.7)> Cu (9.6)> Cr (6.51)> Pb (6.2)> Ni (4.3)> Cd (3.6) when Typha angustifolia sp. and Limnocharis flava sp. were cultivated together; Fe (70.3)> Zn (48.7)> Mg (8.2)> Cu (8.6)> Cr (5.41)> Pb (5.4)> Ni (3.4)> Cd (2.8) when Limnocharis flava sp. was cultivated alone; and Fe (67.3)> Zn (49.7)> Mg (8.1)> Cu (7.6)> Cr (4.51)> Pb (6.4)> Ni (2.9)> Cd (2.3) when Typha angustifolia sp. was cultivated alone. The outcomes clearly exposed the greater sorption capacity of Limnocharis flava
TE D
sp. for all heavy metals except Zn and Pb. Moreover, an obvious improvement in the sorption capability was observed when both plants were employed together. This may be because of the improvement in the uptake performance of the plants. Lee et al. (2014) employed Brassica juncea, Brassica campestris, Sorghum
EP
bicolor, and Helianthus annuus for the removal of Cu, Zn, Cd, and Ni from contaminated soil and observed Cu, Zn, Cd, and Ni accumulations of 14.87 ± 5.1 mg, 11.75 ± 4.3 mg, 49.19 ± 1.2 mg and 4.39 ± 0.5 mg,
AC C
respectively, in plants. While treating mine drain-contaminated soil for the removal of Fe and Al by Phragmites australis, Guo et al. (2014) observed Fe and Al accumulation of 38.46 ± 1.09 mg g-1 and
0.43 ± 0.06 mg g-1 in plants. While removing heavy metals from aqueous solutions with sunflower, potato,
canola and walnut shell residues, Feizi and Jalali (2015) found that the residues had a metal sorption capacity for Fe of up to 40.9 mg g-1 and for Zn of up to 43.2 mg g-1, both of which are lower than our findings. Furthermore, Khokhar et al., 2015 carried out an experiment to remove heavy metal ions with chemically treated Melia azedarach L. 2 leaves and reported that the maximum sorption capacity for Fe (III) by NaOH-treated bio-sorbent was 38.46 mg g-1, while our finding for Fe was 71 mg g-1.
9
ACCEPTED MANUSCRIPT
3.5 SEM study Figure 4 demonstrates the surface features of heavy metal (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd) sorption at a
RI PT
magnification of 100 and 500. The substance has a porous texture with an enormous, reachable surface area that supports metal absorption. The surface of the biomass and pores represent the absorption of heavy
SC
metals (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd).
4. Conclusions
The concrete results of this study revealed that the integrated phytogreen system consisting of two different
M AN U
aquatic plants, namely, Typha angustifolia sp. and Limnocharis flava sp. in a conventional oxidation pond process is a reliable and ecologically attractive option. In particular, maximal heavy metal removal (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd) was realized when Typha angustifolia sp. and Limnocharis flava sp. were cultivated together for a retention time of 13 days. Metal removal efficiency was increased when the combined culture of the two plants was employed in comparison with monoculture, and Limnocharis flava
TE D
sp. showed better performance than Typha angustifolia sp. A positive relation between retention time and heavy metal removal was studied and confirmed by the negative and significant correlation coefficients of the corresponding heavy metals (Fe, Ni, Cu, Zn, Cr, Pb, Mg and Cd) with retention period. The elimination
EP
of the above-mentioned heavy metals was equivalent to their net sorption in plants due to natural precipitation Limnocharis flava sp. showed greater sorption capability than Typha angustifolia sp. for all
AC C
tested heavy metals except Zn and Pb. The scientific contribution of this integrated phytogreen system consisting of two different aquatic plants, namely, Typha angustifolia sp. and Limnocharis flava sp. in the
conventional oxidation pond process may play a role in solving the urgent environmental issues of emission mitigation of heavy metal contamination management. All of the plants used are available free of cost,
making their implementation as absorbents of heavy metals an economically attractive alternative in the
wastewater treatment process. The industrial application of this green technology may make the heavy metal removal process more cost effective.
10
ACCEPTED MANUSCRIPT
Acknowledgements
RI PT
The authors are grateful to the Universiti Malaysia Pahang (UMP), the Faculty of Civil Engineering and Earth Resources (FKASA), Majlis Bandaran Johor Bahru (MBJB), Ranhill Water Services (RWS), Ranhill Utilities Berhad (RUB) and the Danish International Development Agency (DANIDA) for their support. This contemporary investigation was made possible by a grant from the Ministry of Education (MOE)
SC
Malaysia; Fundamental Research Grant Scheme (FRGS) – Vote no: RDU 070108, UMP PreCommercialization Grant – Vote no. UIC 090302 and Prototype Research Grant Scheme (PRGS) – Vote no:
M AN U
RDU120806).
References
TE D
Abhilash, P.C., Pandey, V. C., Srivastava, P., Rakesh, P.S., Chandran, S., Singh, N., Thomas, A.P., 2009. Phytofiltration of cadmium from water by Limnocharis flava (L.) Buchenau grown in freefloating culture system. J. Hazard. Mater. 170, 791–797.
EP
Abid, U., Sun, H., Muhammad, F. H. M., Shah, F., Xiyan, Y., 2015. Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: A review. Environ. Exp. bot. 117, 28-40.
AC C
Ahmadi, A., Heidarzadeh, S., Mokhtari, A. R., Darezereshki, E., Harouni H. A., 2014. Optimization of heavy metal removal from aqueous solutions by maghemite (γ-Fe2O3) nanoparticles using response surface methodology. J. Geochem. Explor. 147, 151-158. Akcil, A., Erust, C., Ozdemiroglu, S., Fonti, V., Beolchini, F., 2015. A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J. Clean. Prod. 86, 24-36. APHA, 2005. Standard methods for the examination of water and wastewater, 20 th ed. Am Public Health Association, Maryland, USA.
11
ACCEPTED MANUSCRIPT
Babu, A. G., Shea, P. J., Sudhakar, D., Jung, I. B., Oh, B. T., 2015. Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal (loid)-contaminated mining site soil. J. Environ. Manage. 151, 160-166.
RI PT
Bah, A. M., Sun, H., Chen, F., Zhou, J., Dai, H., Zhang, G., Wu, F., 2010. Comparative proteomic analysis of Typha angustifolia leaf under chromium, cadmium and lead stress. J. Hazard. Mater. 184, 191–203.
Byungryul, A., Chang, L., Mi-Kyung, S., Jae-Chun, R., Soonjae, L., Seong-Jik, P., Dongye, Z., Song-
SC
Bae, K., Chanhyuk, P., Sang-Hyup, L., Seok, W. H., Jae-Woo, C., 2015. Applicability and toxicity evaluation of an adsorbent based on jujube for the removal of toxic heavy metals. Rea. Func. Pol. 93,
M AN U
138-147.
Cegłowski, M., Schroeder, G., 2015. Preparation of porous resin with Schiff base chelating groups for removal of heavy metal ions from aqueous solutions. Chem. Eng. J. 263, 402-411. Chandra, R., Yadav, S., 2010. Potential of Typha angustifolia for phytoremediation of heavy metals from aqueous solution of phenol and melanoidin. Ecol. Eng. 36, 1277–1284. Deng, G., Li, M., Li, H., Yin, L., Li, W., 2014. Exposure to cadmium causes declines in growth and
TE D
photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). Aquat. Bot. 112, 23-32. Fassett, N.C., Calhoun, B. 1952. Introgression between Typha latifolia and T. angustifolia. Evolution 6, 267-379.
EP
Feizi, M. and Jalali, M., 2015. Removal of heavy metals from aqueous solutions using sunflower, potato, canola and walnut shell residues. J. Taiwan. Inst. Chem. E. 00, 1–12.
AC C
Galal, T. M., Hanaa, S. Shehata, H. S., 2015. Bioaccumulation and translocation of heavy metals by Plantago major L. grown in contaminated soils under the effect of traffic pollution. Ecol. Indic. 48, 244-251.
González, A. G., Cuadros, F., Celma, A. R., Rodríguez, F. L., 2014. Influence of heavy metals in the biomethanation of slaughterhouse waste. J. Clean. Prod. 65, 473-478. Gopal, B., Sharma, K.P. 1980. Aquatic weed control versus utilization. Econ. Bot. 33, 340-346. Grace, J.B., Wetzel, R.G. 1981. Effects of size and growth rate on vegetative reproduction in Typha. Oecologia 50, 158-161.
12
ACCEPTED MANUSCRIPT
Guo, L., Ott, D. W., Cutright, T. J., 2014. Accumulation and histological location of heavy metals in Phragmites australis grown in acid mine drainage contaminated soil with or without citric acid. Environ. Exp. Bot. 105, 46-54.
RI PT
Gustafson, T.D. 1976. Production, photosynthesis and the storage and utilization of reserves in a natural stand of Typha latifolia L. PhD thesis. University of Wisconsin-Madison, 102.
Han, Y., Hwang, G., Kim, D., Park, S., Kim, H., 2015. Porous Ca-based bead sorbents for simultaneous removal of SO2, fine particulate matters, and heavy metals from pilot plant sewage sludge
SC
incineration. J. Hazard. Mater. 283, 44-52.
Hu, Y., Wang, D., Wei, L., Zhang, X., Song, B., 2014. Bioaccumulation of heavy metals in plant leaves
M AN U
from Yan׳an city of the Loess Plateau, China. Ecotox. Environ. Safe. 110, 82-88. Khan, E., Khaodhir, S., Ruangrote, D., 2009. Effects of moisture content and initial pH in composting process on heavy metal removal characteristics of grass clipping compost used for storm water filtration. Bioresour. Technol. 100, 4454-4461.
Khokhar, A., Siddique, Z., Misbah, 2015. Removal of heavy metal ions by chemically treated Melia azedarach L. 2 leaves. J. Environ. Chem. Eng. doi:10.1016/j.jece.2015.03.009.
TE D
Ladislas, S., Gérente, C., Chazarenc, F., Brisson, J., Andrès, Y., 2014. Floating treatment wetlands for heavy metal removal in highway stormwater ponds. Ecol. Eng. doi:10.1016/j.ecoleng.2014.09.115. Lara, M. A. M., Blázquez, G., Trujillo, M.C., Pérez, A., Calero, M., 2014. New treatment of real
EP
electroplating wastewater containing heavy metal ions by adsorption onto olive stone. J. Clean. Prod. 81, 120-129.
AC C
Lee, J., Sung, K., 2014. Effects of chelates on soil microbial properties, plant growth and heavy metal accumulation in plants. Ecol. Eng. 73, 386-394. Liu, W. J., Zeng, F. X., Jiang, H., Zhang, X. S., 2011. Adsorption of lead (Pb) from aqueous solution with Typha angustifolia biomass modified by SOCl2 activated EDTA. Chem. Eng. J. 170, 21–28. Marchand, L., Nsanganwimana, F., Oustrière, N., Grebenshchykova, Z., Allende, K. L., Mench, M., 2014. Copper removal from wastewater using a bio-rack system either unplanted or planted with Phragmitesaustralis, Juncus articulates and Phalaris arundinacea. Ecol. Eng. 64, 291–300.
13
ACCEPTED MANUSCRIPT
Matouq, M., Jildeh, N., Qtaishat, M., Hindiyeh, M., Syouf, M.Q.A., 2015. The adsorption kinetics and modeling for heavy metals removal from wastewater by Moringa pods. J. Environ. Chem. Eng. 3, 775784.
RI PT
Mendoza, R. E., García, I. V., Cabo, L. D., Weigandt, C. F., Iorio, A. F. D., 2015. The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River Basin (Argentina). Sci. Total Environ. 505, 555-564.
Mesa, J., Naranjo, E. M., Caviedes, M.A., Gómez, S. R., Pajuelo, E., Llorente, I. D. R., 2015. Scouting
SC
contaminated estuaries: Heavy metal resistant and plant growth promoting rhizobacteria in the native metal rhizoaccumulator Spartina maritima. Mar. Pollut. Bull. 90, 150-159.
M AN U
Mohammad, I. A., Adel, R. A. Usman, Ahmed, H. E., Anwar, A. A., Hesham, M. I., Salem, E., Abdulrasoul, A., 2015. Conocarpus biochar as a soil amendment for reducing heavy metal availability and uptake by maizeplants. Saudi. J. biol. sci. 22, 503-511.
Morteza, F., Mohsen, J., 2015. Removal of heavy metals from aqueous solutions using sunflower,
Nguyen,
canola and walnut shell residues. J. Taiwan Inst. Chem. E. doi:10.1016/j.jtice.2015.03.027.
V.
TE D
potato,
K.,
Lee,
J.U.,
2015.
Effect of sulfur
concentration on microbial
removal of arsenic and heavy metals from mine tailings using mixed culture of Acidithiobacillus spp. J. Geochem. Explor. 148, 241-248.
EP
Oosten, M. J. V., Maggio, A., 2015. Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ. Exp. Bot. 111, 135-146.
AC C
Philippe, A. G., Masotti, V., Höhener, P., Boudenne, J. L., Viglione, J., Schwob, I. L., 2014. Constructed wetlands to reduce metal pollution from industrial catchments in aquatic Mediterranean ecosystems: A review to overcome obstacles and suggest potential solutions. Environ. Int. 64, 1-16. Ponce, S. C., Prado, C., Pagano, E., Prado, F. E., Rosa, M., 2015. Effect of solution pH on the dynamic
of biosorption of Cr (VI) by living plants of Salvinia minima. Ecol. Eng. 74, 33-41. Pratas, J., Paulo, C., Favas, P. J. C., Venkatachalam, P., 2014. Potential of aquatic plants for phytofiltration of uranium-contaminated waters in laboratory conditions. Ecol. Eng. 69, 170-176.
14
ACCEPTED MANUSCRIPT
Rezania, S., Ponraj, M., Talaiekhozani, A., Mohamad, S. E., Din, M. F. M., Taib, S. M., Sabbagh, F., Sairan, F. M. 2015. Perspectives of phytoremediation using water hyacinth for removal of heavy metals, organic and inorganic pollutants in wastewater. J. Environ. Manage. 163, 125-133.
RI PT
Rodolfo, E. M., Ileana, V. G., Laura, D. C., Cristian, F. W., Alicia, F. D. I., 2015. The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River Basin (Argentina). Sci. total. environ. 505, 555-564.
Said, M., Cassayre, L., Dirion, J. L., Nzihou, A., Joulia, X. 2015. Behavior of heavy metals during
SC
gasification of phytoextraction plants: thermochemical modelling. Compu. Aid. Chem. Eng. 37, 341346.
M AN U
Sargın, İ., Kaya, M., Arslan, G., Baran, T., Ceter, T., 2015. Preparation and characterisation of biodegradable pollen–chitosan microcapsules and its application in heavy metal removal. Bioresour. Technol. 177, 1-7.
Shavandi, M.A., Haddadian, Z., Ismail, M.H.S., Abdullah, N., Abidin, Z.Z., 2012. Removal of Fe (III), Mn(II) and Zn(II) from palm oil mill effluent (POME) by natural zeolite. J. Taiwan Inst. Chem. E. 43, 750-759.
TE D
Siddique, M.N. I., Munaim, M.S.A, Zularisam, A.W., 2014. Feasibility analysis of anaerobic codigestion of activated manure and petrochemical wastewater in Kuantan (Malaysia). J. Clean. Prod., In Press, Accepted Manuscript, Available online 19 August 2014, doi:10.1016/j.jclepro.2014.08.003.
EP
Smain, M., Saida, S., Michel, C., 2009. Toxicity and removal of heavy metals (cadmium, copper, and zinc) by Lemna gibba. Ecotox. Environ. Safe. 72, 1774-1780.
AC C
Smith, S.G., 1962. Natural hybridization among five species of cattail. Am. J. Bot. 49, 678. Syukor, A.R., Zularisam, A.W., Zakaria, I., Ismid, M., Sulaiman, S., Halim, A., Thomas, D. L., 2013. Potential of Aquatic Plant as Phytoremediator for Treatment of Petrochemical Wastewater in Gebeng Area, Kuantan. Adv. Environ. Biol. 7, 3808–3814. Syukor, A.R., Zularisam, A.W., Ideris, Z., Ismid, M.S. M., Nakmal, H.M., Sulaiman, S., Hasmanie, A.H., Norsita, M.R.S., Nasrullah, M., 2014. Performance of Phytogreen Zone for BOD5 and SS Removal for Refurbishment Conventional Oxidation Pond in an Integrated Phytogreen System. Int. J. Environ. Ear. Sci. Eng. 8, 164-169.
15
ACCEPTED MANUSCRIPT
Taylor, Crowder, 1984. Cooper and Nickel tolerance in T. latifolia clones from contaminated and uncon. envir. Can J. Bot. 62, 1304-1308. Wilcox, D.A., Apfelbaum, S.I., R. Hiebert. 1984. Cattail invasion of sedge meadows following
Soc. of Wetlands Scientists 4, 115-128.
RI PT
hydrologic disturbance in the Cowles Bog Wetland Complex, Indiana Dunes National Lakeshore. J.
Xu, W., Shi, W., Yan, F., Zhang, B., Liang, J., 2011. Mechanisms of cadmium detoxification in cattail (Typha angustifolia L.). Aquat. Bot. 94, 37–43.
SC
Zhu, C., Tian, H., Cheng, K., Liu, K., Wang, K., Hua, S., Gao, J., Zhou, J., 2015. Potentials of whole process control of heavy metals emissions from coal-fired power plants in China. J. Clean. Prod., in
AC C
EP
TE D
M AN U
Press, Corrected Proof, Available online 21 May 2015, doi:10.1016/j.jclepro.2015.05.008.
16
ACCEPTED MANUSCRIPT
Characteristics of wastewater obtained from four stations (S1- S4) S3
S4
847±0.9 292±0.64 1.86±0.05 7.79±0.01 30.8±0.15 0.45±0.001 14±0.02 17±0.01 0.23±0.002 0.05±0.001 0.35±0.002 0.3±0.002 0.32±0.002 0.16±0.001 0.22±0.002 0.3±0.002
848±1 293±0.7 1.87±0.06 7.8±0.01 30. 85±0.28 0.46±0.001 15±0.02 18±0.01 0.24±0.002 0.06±0.001 0.4±0.003 0.35±0.003 0.38±0.003 0.17±0.001 0.23±0.002 0.29±0.002
846±0.9 291±0.6 1.85±0.05 7.78±0.01 29.9±0.17 0.44±0.001 13±0.01 16±0.01 0.22±0.001 0.04±0.001 0.29±0.001 0.24±0.001 0.27±0.001 0.15±0.001 0.21±0.001 0.28±0.001
845±0.8 290±0.53 1.84±0.04 7.77±0.01 29.4±0.14 0.43±0.001 12±0.01 15±0.01 0.21±0.001 0.03±0.001 0.2±0.001 0.20±.001 0.250±.001 0.14±0.001 0.2±0.001 0.27±0.001
EP
TE D
M AN U
S2
AC C
COD (mgL-1) BOD (mgL-1) DO (mgL-1) pH Temperature (ºC) Conductivity (mScm-1) Nitrate (mgL-1) Phosphorous (mgL-1) Pb (mgL-1) Cd (mgL-1) Cr (mgL-1) Cu (mgL-1) Mg (mgL-1) Ni (mgL-1) Zn (mgL-1) Fe (mgL-1)
S1
SC
Table1
RI PT
List of Tables
Values are the mean + S.E. of the 4 replicates
1
ACCEPTED MANUSCRIPT
Table2
Heavy metals (%)
Plant mean
S2
S3
S4
Lim
56.3±0.2a 55.3±0.2a 54.6±0.3a 53.7±0.2a 49.5±0.2a 45.2±0.3a 44.2±0.3a 43.3±0.3a
57.7±0.2b 56.7±0.2b 57.4±0.3b 57.1±0.2b 52.3±0.2b 47.2±0.3b 46.2±0.3b 46.4±0.3b
61.2±0.2c 60.2±0.2c 60.3±0.3c 59.2±0.2c 55.4±0.3c 51.5±0.3c 50.5±0.3c 46.7±0.3c
62.4±0.2d 61.4±0.2d 63.4±0.3d 60.5±0.2d 57.5±0.2d 52.4±0.3b 51.4±0.3b 48.5±0.3d
57.6±0.2b 56.6±0.2b 58.2±0.2b 56.2±0.2b 52.4±0.2b 46.3±0.2b 45.3±0.2b 44.4±0.3b
Typ
Lim+ Typ
53.7±0.2a 52.7±0.2a 52.3±0.2a 53.4±0.2a 46.5±0.2a 41.1±0.2a 40.1±0.2a 40.5±0.3a
63.2±0.2c 62.2±0.2c 61.8±0.2c 59.6±0.2c 58.3±0.2c 54.7±0.2c 53.7±0.2c 49.3±0.3c
SC
S1
M AN U
Fe Ni Cu Zn Cr Pb Mg Cd
Station mean
RI PT
Assessment of heavy metal removal efficiency between stations and plants
AC C
EP
TE D
The values followed by same letter are not significantly different at the 0.05 probability level. Lim = Limnocharis flava sp. and Typ = Typha angustifolia sp.
2
ACCEPTED MANUSCRIPT
Table 3 The relationship between retention time and heavy metal removal at p<0.05
Zn
Cr
Pb
Mg
Cd
Correlation coefficient S4
Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ
-0.84 -0.90 -0.91 -0.94 -0.92 -0.93 -0.93 -0.91 -0.94 -0.93 -0.90 -0.97 -0.97 -0.90 -0.89 -0.98 -0.95 -0.87 -0.94 -0.92 -0.95 -0.89 -0.95 -0.92
-0.98 -0.94 -0.91 -0.92 -0.98 -0.93 -0.96 -0.94 -0.96 -0.87 -0.93 -0.92 -0.90 -0.92 -0.86 -0.97 -0.96 -0.97 -0.97 -0.95 -0.97 -0.86 -0.84 -0.88
-0.91 -0.88 -0.97 -0.80 -0.96 -0.94 -0.93 -0.87 -0.89 -0.92 -0.98 -0.95 -0.80 -0.95 -0.88 -0.92 -0.84 -0.94 -0.94 -0.88 -0.90 -0.93 -0.36 -0.96
-0.87 -0.90 -0.92 -0.91 -0.92 -0.94 -0.84 -0.89 -0.89 -0.98 -0.88 -0.90 -0.99 -0.99 -0.95 -0.92 -0.93 -0.94 -0.85 -0.90 -0.90 -0.86 -0.87 -0.96
SC
RI PT
Correlation coefficient S3
M AN U
Cu
Correlation coefficient S2
TE D
Ni
Correlation coefficient S1
EP
Fe
Plants
AC C
Heavy metals
3
ACCEPTED MANUSCRIPT
Table 4 Mass Balance calculations of heavy metals in Limnocharis flava sp., Typha angustifolia sp. and their combination (retention period 13 days)
Zn
Cr
Pb
Mg
Cd
R (mg)
Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ Lim+ Typ Lim Typ
7.3±0.23 7.3±0.23 7.3±0.23 4.46±0.08 4.46±0.08 4.46±0.08 5.54±0.15 5.54±0.15 5.54±0.15 6.09±0.24 6.09±0.24 6.09±0.24 7.14±0.08 7.14±0.08 7.14±0.08 3.04±0.08 3.04±0.08 3.04±0.08 5.57±0.15 5.57±0.15 5.57±0.15 3.99±0.12 3.99±0.12 3.99±0.12
1.46±0.07 2.04±0.17 2.49±0.16 1.18±0.05 1.48±0.1 1.73±0.09 1.29±0.17 1.74±0.18 1.86±0.17 1.5±0.14 1.83±0.15 1.71±0.08 2.27±0.18 2.57±0.08 3.09±0.07 0.98±0.08 1.12±0.1 1.42±0.08 1.3±0.17 1.76±0.18 1.86±0.17 1.59±0.13 1.69±0.23 2.02±0.13
4.29±0.15 3.71±0.16 3.26±0.21 2.55±0.09 2.25±0.09 2±0.08 2.52±0.38 2.07±0.37 1.95±0.36 3.49±0.39 3.16±0.49 3.28±0.37 3.79±0.17 3.49±0.07 2.97±0.08 1.63±0.09 1.49±0.17 1.19±0.1 2.53±0.38 2.07±0.37 1.97±0.36 1.75±0.04 1.65±0.33 1.32±0.33
1.55±0.09 1.55±0.09 1.55±0.09 0.73±0.08 0.73±0.08 0.73±0.08 1.73±0.08 1.73±0.08 1.73±0.08 1.1±0.18 1.1±0.18 1.1±0.18 1.08±0.11 1.08±0.11 1.08±0.11 0.43±0.08 0.43±0.08 0.43±0.08 1.74±0.08 1.74±0.08 1.74±0.08 0.65±0.28 0.65±0.28 0.65±0.28
SC
RI PT
Net amount absorbed by plants (mg)
M AN U
Cu
Effluent concentration (mg)
TE D
Ni
Influent concentration (mg)
EP
Fe
Plants
AC C
Heavy metals
Values are the mean + S.E. of the 4 observations, Lim = Limnocharis flava sp. and Typ = Typha angustifolia sp.R=Heavy metal removal by natural degradation in control
4
ACCEPTED MANUSCRIPT
M AN U
SC
RI PT
List of Figures
AC C
EP
TE D
Fig. 1. Layout of experimental set up, where influent zone (Z1), Phytogreen zone (Z2), Aeration zone (Z3), Inclined Plate Clarifier zone (Z4) and effluent zone (Z5); S1-S15 in-situ sampling points.
1
AC C
EP
TE D
Fig. 2. Photograph of experimental set up.
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
2
ACCEPTED MANUSCRIPT
SC
RI PT
Fe removal from station 1 (S1) wastewater
M AN U
a
AC C
b
EP
TE D
Fe removal from station 2 (S2) wastewater
3
ACCEPTED MANUSCRIPT
SC
RI PT
Fe removal from station 3 (S3) wastewater
M AN U
c
AC C
d
EP
TE D
Fe removal from station 4 (S4) wastewater
Fig. 3. (a-d) Effect of Typha angustifolia sp., Limnocharis flava sp. and their combination on Fe concentrations of S1 to S4 wastewater , where Typ = Typha angustifolia sp, Lim = Limnocharis flava sp.
4
ACCEPTED MANUSCRIPT
a
M AN U
SC
RI PT
b
d
AC C
EP
TE D
c
Fig. 4. SEM of (a, c) heavy metals loaded dried (Thypha angustifolia) biomass (b, d) heavy metals loaded dried (Limnocharis flava) biomass ×100 and 500.
5
ACCEPTED MANUSCRIPT
Highlights
The combination of Limnocharis flava and Typha angustifolia improved heavy metal removal.
RI PT
•
A longer retention period improved Heavy metal removal.
•
The removal of heavy metals was equivalent to their net sorption in plants
•
Limnocharis flava sp. exhibited greater metal sorption capacities
AC C
EP
TE D
M AN U
SC
•