Bioresource Technology 92 (2004) 197200

Heavy metal adsorption properties of a submerged aquatic plant (Ceratophyllum demersum)

c,*

Department of Environmental Engineering, Faculty of Engineering, Cukurova University, 01330 Balcali-Adana, Turkey b Fisheries Faculty, Cukurova University, 01330 Balcali-Adana, Turkey c Department of Civil Engineering, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK Received 25 April 2003; received in revised form 23 June 2003; accepted 27 July 2003

Abstract Heavy metals can be adsorbed by living or non-living biomass. Submerged aquatic plants can be used for the removal of heavy metals. In this paper, lead, zinc, and copper adsorption properties of Ceratophyllum demersum (Coontail or hornwort) were investigated and results were compared with other aquatic submerged plants. Data obtained from the initial adsorption studies indicated that C. demersum was capable of removing lead, zinc, and copper from solution. The metal biosorption was fast and equilibrium was attained within 20 min. Data obtained from further batch studies conformed well to the Langmuir Model. Maximum adsorption capacities (qmax ) onto C. demersum were 6.17 mg/g for Cu(II), 13.98 mg/g for Zn(II) and 44.8 mg/g for Pb(II). Kinetics of adsorption of zinc, lead and copper were analysed and rate constants were derived for each metal. It was found that the overall adsorption process was best described by pseudo second-order kinetics. The results showed that this submerged aquatic plant C. demersum can be successfully used for heavy metal removal under dilute metal concentration. 2003 Elsevier Ltd. All rights reserved.
Keywords: Aquatic plants; Biosorption; Heavy metals; Langmuir model; Pseudo second-order

1. Introduction Heavy metals pose serious environmental risks and, therefore, their removal from wastewaters, particularly, has been examined extensively. A range of methods has been used for heavy metal removal and one of the most common methods is adsorption, with activated carbon being the most widely used adsorbent for this purpose. However, this can be expensive and there has been considerable interest in the use of other adsorbent materials, particularly biosorbents (Wase and Forster, 1997; Ajmal et al., 2000). It has long been known that aquatic plants, both living and dead, are heavy metal accumulators and, therefore, the use of aquatic plants for the removal of heavy metals from wastewater has gained high interest (Kuyucak and Volesky, 1989). Some freshwater macrophytes including Potamogeton lucens, Salvinia herzogoi, Eichhornia crassipes, Myrio-

phyllum brasillensis, Myriophyllum spicatum, Cabomba sp., Ceratophyllum demersum have been investigated for the removal of heavy metals (Wang et al., 1996; Schneider and Rubio, 1999; Schneider et al., 1999; Keskinkan et al., 2003). The removal of metals by biosorption and the mechanisms of biosorption have been discussed previously and it has been reported that biosorption may be classied as being: extracellular accumulation/precipitation, cell surface sorption/precipitation, and intracellular accumulation (Veglio and Beolchini, 1997) and can occur by complexation, co-ordination, chelation of metals, ion exchange, adsorption and micro precipitation (Wang et al., 1996). The bioremoval process using aquatic plants contains two uptake processes: an initial fast, reversible, metal-binding processes (biosorption); a slow, irreversible, ion-sequestration step (bioaccumulation). Schneider et al. (1999) have studied the biosorption of metals onto plant biomass in order to determine whether

* Corresponding author. Tel.: +44-121-414-5049; fax: +44-121-4143675. E-mail address: [email protected] (C.F. Forster).

0960-8524/$ - see front matter 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2003.07.011

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it was exchange adsorption or surface precipitation. It was found that the sorption was a function of pH and was greatest at a pH value which was slightly more acidic than the pH at which there was bulk precipitation of the metal hydroxide. These workers have also studied the t, or approximate t, of the sorption data to the Langmuir isotherm. This was considered to be evidence that sorption stopped at one monolayer, consistent with specic and strong sorption onto specic sites. C. demersum (Coontail or hornwort) is a completely submersed plant and commonly seen in ponds, lakes, ditches, and quiet streams with moderate to high nutrient levels (Johnson et al., 1995). It does not produce roots, instead it absorbs all the nutrients it requires from the surrounding water. If it is growing near the lake bottom, it will form modied leaves, which it uses to anchor to the sediment. However, it can oat free in the water column and sometimes forms dense mats just below the surface. The main purpose of this study, therefore, is to investigate the adsorption characteristics of zinc, copper, and lead onto C. demersum.

experiments were duplicated and the results presented as mean values. The variation was <5%.

3. Results and discussion 3.1. Basic adsorption According to Schneider et al. (2001) who have provided an extensive discussion of the eect of pH on heavy metal biosorption, at slightly acidic pH values, M2 concentrations were highest and suitable for metal adsorption. In this current work, pH values were just below 6 indicating that there was a suitable environment for metal adsorption by C. demersum. The initial adsorption tests for zinc, lead and copper showed that C. demersum would adsorb all three metals (Fig. 1). The data also showed that a contact time of 20 min was sucient to achieve equilibrium. Further adsorption tests were then carried out and when the data were plotted as Ce =qe against Ce , the linearised form of the Langmuir equation, good straight lines were obtained which is considered to be evidence that sorption was as a monolayer. The regression equations were signicant at the 99% level. The qmax values were found to be 44.8, 13.98 and 6.17 mg g1 for lead, zinc and copper respectively (Table 1). Schneider and Rubio (1999) have reported that they obtained low metal adsorption results with C. demersum compared to other aquatic plants. However, it is not possible to compare the current qmax values with their results, as they did not carry out further experiments in order to obtain qmax values for each metal. Table 1 also compares the qmax values from the current research with those obtained for other aquatic plants by various workers and shows that the performance of C. demersum was comparable with that of the other aquatic plants, with the exception of P. lucens, for lead and zinc. However, its capacity for adsorbing copper was not as good as the others. Work on

2. Methods The plant biomass was collected locally and consisted of the oating part of the plant. After it had been harvested, it was washed with dilute hydrochloric acid (3%) and distilled water before being used. Analytical grade copper(II) sulphate, zinc(II) sulphate and lead(II) nitrate were used as the metal sources and stock solutions of these metal ions were prepared in deionised water. The sorption tests were conducted at 25 C in conical asks (250 ml) using an orbital shaker in a constant room temperature. The initial pH values were between 5 and 6 during the batch experiments and no pH adjustment was made. Therefore, all the sorption experiments were carried out at pH values of <6. C. demersum biomass (about 2 g wet weight) was added to each ask and placed on the orbital shaker. The initial metal concentration for the contact time experiments was 10 mg/l and the incubation times ranged from 5 to 160 min. The data used to derive the Langmuir constants were obtained by using C. demersum biomass (about 2 g wet weight) and metals concentrations of 2, 4, 8, 16, 32 and 64 mg/l. The contact time was 120 min. After contacting, the contents of the ask were ltered to separate the biomass from the solution. The ltrates were then analysed with an atomic absorption spectrophotometer (Perkin Elmer model 3100) to determine the metal concentrations in the samples. Control experiments were performed for each metal to measure any adsorption onto the glassware. Neither precipitation nor adsorption onto the walls of the asks was observed. The results of metal analysis were used to calculate the specic adsorption (mg metal adsorbed/g of biomass, dry weight). All the

5 4.5 4 3.5 3 2.5 2 1.5 1 0.5 0 0 50 100 150 200

Specific adsorption (mg/g)

Time (min)
Fig. 1. Initial adsorption isotherm for zinc (r), lead (N) and copper (j) onto C. demersum.

O. Keskinkan et al. / Bioresource Technology 92 (2004) 197200 Table 1 A comparison of the heavy metal uptake capacities (qmax , mg/g) of various macrophytes Adsorbent Ceratophyllum demersum (this study) Myriophyllum spicatum (Keskinkan et al., 2003) Myriophyllum spicatum (Wang et al., 1996) Potamogeton lucens (Schneider et al., 1999) Salvinia herzegoi (Schneider et al., 1999) Eichhornia crassipes (Schneider et al., 1999) Lead 44.8 (R2 0:97) 46.69 55.6 141 Zinc 13.98 (R2 0:97) 15.59 13.5 32.4 18.1 19.2 Copper 6.17 (R2 0:97) 10.37 12.9 40.8 19.7 23.1

199

Specific adsorption (mg/g)

the adsorption of heavy metals by Spirulina sp. has shown that the chemical composition of the cells did aect the degree of adsorption which occurred, with Cr(VI) being less readily adsorbed when there was a high concentration of polysaccharides in the cells (Hernandez and Olguin, 2002). It is recognised that Spirulina is an algal species, not an aquatic plant, but it is a worthwhile comparison and points to an area which needs evaluation. 3.2. Kinetics of adsorption If the movement of the solute from the bulk liquid lm surrounding the adsorbent is ignored, the adsorption process for porous solids can be separated into three stages: mass transfer (boundary layer diusion), sorption of ions onto sites, intraparticle diusion. External mass transfer is characterised by the initial rate of solute adsorption. This can be calculated from the initial slope of the Ct =C0 time curves. These slopes can be derived by assuming that the relationship was linear over the rst 510 min (McKay et al., 1982). This gave initial rates of 0.094, 0.0715 and 0.0652 min1 for lead, zinc and copper respectively. In many cases, there is the possibility that intraparticle diusion will be the rate limiting step and this is normally determined by using the equation described by Weber and Morris (1963): q kp 1=2 t where q is the amount of the metal adsorbed at time t, (mg/g); kp the intraparticle rate constant (mg/g min0:5 ). Fig. 2 shows that the relationships for C. demersum and copper zinc, lead systems are not linear over the entire time range, indicating that more than one process is aecting the adsorption. This type of non-linearity has been reported previously by various authors (Keskinkan et al., 2003; McKay et al., 1980; Ho et al., 1996; Fernandez et al., 1996) and has been interpreted as showing that both boundary layer diusion, the initial curved portion, and intraparticle diusion, the nal

5 4.5 4 3.5 3 2.5 2 1.5 1 0.5 0 0 2 4 6 8 10 12 14

Time0.5 (min0.5)
Fig. 2. Plots for the intraparticle diusion for zinc (r), lead (N) and copper (j) onto C. demersum.

linear portion, are occurring. The slope of the nal linear portion can be used to derive a rate parameter, kp , for intraparticle diusion. It is also possible to derive an initial rate parameter, j, by linear regression between t 0 and tlim which is the rst breakpoint in the relationship (Ho et al., 1996). Values for these parameters are given in Table 2. These rate parameters have units of mg/g min0:5 and, as such, are not a direct quantication of the rates. Nevertheless, they can be interpreted in relative terms. According to the theoretical equations for diusion, when intraparticle diusion is the only rate-determining step, the rate parameter is directly related to the square root of the initial concentration (Ho et al., 1996). That is to say; j C0 n where n 0:5. However, values for n were found to be 0.043 for zinc, 0.0098 for copper and 0.177 for lead. This conrms that intraparticle diusion was not the only operative mechanism and not the rate-determining step for the lead, copper, zinc and C. demersum systems.

Table 2 Rate constants for each metal (mg/g min0:5 ) Metal Initial rate constant, kp (mg/g min0:5 ) 1.103 1.023 1.506 R2 Pseudo constants, second-order (g/mg min) rate 0.0147 0.1834 0.0137 R2

Zinc Copper Lead

0.995 0.986 0.970

0.999 0.999 0.999

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In many cases, the kinetics of adsorption by any biological material have been only tested for the rst-order expression given by Lagergren. However, it has also been shown that a pseudo second-order approach can sometimes provide a better description of the adsorption kinetics (Cheung et al., 1997). The rst-order Lagergren equation is: lnqe qt lnqe Kt The pseudo second-order equation is: t =qt b 1=2 K 0 q2 e c t =qe where qe is the mass of metal adsorbed at equilibrium (mg/g), qt the mass of metal adsorbed at time t (mg/g), K is the rst-order reaction rate constant of adsorption (min1 ), K 0 the pseudo second-order rate constant of adsorption (g/mg min). It was found that, although the rst-order equation was suitable for some of the data, it was not applicable for all the results. Therefore, no further consideration was given to it. The pseudo second-order reaction model, however, was applicable to all the data and values of the reaction rate constants and correlation coecients for each metal are listed in Table 2.

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Ajmal, M., Rao, A.K.R., Rais, A., Jameel, A., 2000. Adsorption studies on Citrus reticulata (fruit peel of orange): removal and recovery of Ni(II) from electroplating wastewater. J. Haz. Mater. B 79, 117131. Cheung, C.W., Porter, C.F., McKay, G., 1997. Sorption kinetics for the removal of copper and zinc from euents using bone char. Sep. Purif. Technol. 19, 5564. Fernandez, N., Chacin, C., Garcia, C., Alastre, N., Leal, F., Forster, C.F., 1996. The use of seed pods from Albizia lebbek for the removal of alkyl benzene sulphonates from aqueous solution. Process Biochem. 32, 383387. Hernandez, E., Olguin, E.J., 2002. Biosorption of heavy metals inuenced by the chemical composition of Spirulina sp. (Arthrospira) biomass. Environ. Technol. 23, 13691377. Ho, Y.S., Wase, D.A.J., Forster, C.F., 1996. Kinetic studies of competitive heavy metal adsorption by sphagnum moss peat. Environ. Technol. 17, 7177. Johnson, D., Kershaw, L., MacKinnon, A., Pojar, J., 1995. Plants of Western Boreal Forest and Aspen Parkland. Lone Pine publishing, Vancouver, BC. Keskinkan, O., Goksu, M.Z.L., Yuceer, A., Basibuyuk, M., Forster, C.F., 2003. Heavy metal adsorption characteristics of a submerged aquatic plant (Myriophyllum spicatum). Process Biochem., in press. Kuyucak, N., Volesky, B., 1989. Biosorbents for recovery of metals from industrial solutions. Biotechnol. Lett. 10, 137142. McKay, G., Blair, H.S., Gardner, J.R., 1982. Adsorption of dyes on chitin. 1. Equilibrium studies. J. Appl. Polmer Sci. 27, 30433047. McKay, G., Otterburn, M.S., Sweeney, A.G., 1980. The removal of colour from euent using various adsorbentsIII silica rate processes. Water Res. 14, 1520. Schneider, I.A.H., Rubio, J., 1999. Sorption of heavy metal ions by the non-living biomass of freshwater macrophytes. Environ. Sci. Technol. 33, 22132217. Schneider, I.A.H., Rubio, J., Smith, R.W., 1999. Eect of some mining chemicals on biosorption of Cu(II) by the non-living biomass of the freshwater macrophyte Potamogeton lucens. Miner. Engng. 12, 255260. Schneider, I.A.H., Rubio, J., Smith, R.W., 2001. Biosorption of heavy metals onto plant biomass: exchange adsorption or surface precipitation? Int. J. Mineral Process. 62, 111120. Veglio, F., Beolchini, F., 1997. Removal of heavy metal ions by biosorption: A review. Hydrometallurgy 44, 301316. Wang, T.C., Weissman, J.C., Ramesh, G., Varadarajan, R., Benemann, J.R., 1996. Parameters for removal of toxic heavy metals by water milfoil (Myriophyllum spicatum). Bull. Environ. Contamin. Toxicol. 57, 779786. Wase, D.A.J., Forster, C.F., 1997. Biosorbents for Metal Ions. Taylor and Francis, London. Weber, W.J., Morris, J.C., 1963. Kinetics of adsorption on carbon from solutions. J. Sanit. Engng. Div. Am. Soc. Civ. Eng. 89, 3160.

4. Conclusions From the work presented here, the aquatic submerged plant C. demersum can be an eective biosorbent for zinc, lead copper removal under dilute metal conditions. Batch adsorption studies showed that C. demersum would adsorb zinc, lead and copper and that, based on the Langmuir coecients, the maximum adsorption capacity was 13.98 mg/g for zinc, 44.80 mg/g for lead and 6.17 mg/g for copper. The initial part of the adsorption was governed by a rst degree lm diusion process. The data also conrm that intraparticle diusion was not the rate-determining step. The overall adsorption rate showed that the zinc, copper and lead and C.demersum system was best described by the pseudo second-order model.