Marine Macrophytes asEffective Lead Biosorbents

Chiara Pennesi1*, Cecilia Totti1, Tiziana Romagnoli1, Barbara Bianco2,Ida De Michelis2, Francesca Beolchini1

ABSTRACT: Several species of seagrass and marine macrophytes wereinvestigated for their biosorption performance in the removal of leadfrom aqueous solution. The effect of pH on the equilibrium of theseagrass Cymodocea nodosa as a biosorbent also was studied. It wasfound that increasing pH increased lead biosorption, with a maximumuptake of approximately 140 mg/g in the range pH 3.3 to 5. Equilibriumdata at different pH levels were successfully fitted to competitiveequilibrium models. In addition, the seaweeds belonging to differentphyla (i.e., Chlorophyta, Heterokontophyta, and Rhodophyta) werestudied for the effect of their structure on equilibrium at a constantpH 5. The brown algae (Heterokontophyta) showed the highest potentialfor lead sorption, with a maximum uptake of 220 mg/g for C. compressaand 140 mg/g for S. lomentaria. The green algae (Chlorophyta) showedlead uptake in the range 40 to 90 mg/g, and the red algae (Rhodophyta)was least effective, with uptake in the range 10 to 40 mg/g. WaterEnviron. Res., 84, 9 (2012).

KEYWORDS: algae, Cymodocea nodosa, Langmuir equilibrium mod-eling, lead biosorption, seagrass.

doi:10.2175/106143011X12989211841296

IntroductionBiosorption typically refers to the metabolism-independent

binding of heavy metals by living or dead biomass. This processcan be used to remove toxic metals from metal-containingindustrial wastewaters. In fact, the passive potential of metalbiosorption by biomass materials has been well-established inthe last twenty years (Veglio and Beolchini, 1997; Volesky, 1990).For economic reasons, particular attention has to be paid toabundant biomass types including those that are generated asa waste product of large-scale industrial fermentations or thosethat are found in large quantities in the sea such as certainmetal-binding macrophytobenthos (Lee and Volesky, 1997).Among the huge diversity of biomass available, seagrasses andmarine algae have proved to be promising for use in heavy-metalrecovery because of their cheap availability, relatively highsurface area, and high binding affinity (Cengiz et al., 2008;Klimmek et al., 2001; Lee and Volesky, 1997; Ghimire at al.,2008; Murphy et al., 2008; Tien, 2002; Vijayaraghavan et al.,

2008; Yun et al., 2001). Seaweeds have been reported to possessa high metal-binding capacity in part because of their cell wall,which has an important role in metal binding (Davis et al., 2003;Schiewer and Wong, 2000; Schiewer and Volesky, 2000; Shenget al., 2004). The Heterokontophyta algal matrix (i.e., brownalgae) is predominately alginic acid with carboxyl groups anda smaller amount of sulfated polysaccharide such as fucoidanwith sulfonic acid. Rhodophyta (i.e., red algae) contain a numberof sulfated galactans (e.g., agar, carregeenan, porphyran, andfurcelleran). Chlorophyta (i.e., green algae) may have anexternal capsule that is composed of protein or polysaccharidesor both.

Seagrasses have not been as well studied for their ability asa metal sorbent. Sanchez et al. (1999) studied copper and zincsorption by Cymodocea nodosa (Ucria) Ascherson (i.e., phylumMagnoliophyta). They found that optimal biosorption of heavymetal occurs because of the chemical composition of the externallayer that covers the leaves known as the cuticle (Sanchez et al.,1999). The cuticle consists of cutin, which is composed of omegahydroxy acids and their derivatives interlinked via ester bonds andforming a polyester polymer of indeterminate size (Benavente etal., 1998). This amorphous substance likely is responsible for thechemical and physical bond with heavy metal through itscarboxylic groups.

In this paper, the influence of pH on lead equilibrium uptakeby a biomaterial consisting of dried C. nodosa was studied. Twoequilibrium sorption models, which take into account thecompetition between hydrogen and metal ions, were successfullyapplied to the experimental data: the ideal competitiveadsorption Langmuir model (ICA) and the non-ideal compet-itive adsorption model (NICA). The binding of lead ions by sixseaweeds and by one seagrass also was investigated to find anymorphological effect on the process: Cystoseira compressaGerloff & Nizamuddin; Scytosiphon lomentaria (Lyngbye) Link(Heterokontophyta); Ulva compressa Linnaeus; Ulva rigida C.Agardh (Chlorophyta); Gracilaria bursa-pastoris (S.G. Gmelin)P.C. Silva; Porphyra leucosticta Thuret; Polysiphonia sp.(Rhodophyta); and Cymodocea nodosa (Magnoliophyta).

MethodologyMarine Macrophyte Sampling and Preparation. The

biosorbent materials used were obtained from several species ofmarine seaweeds and seagrasses that were sampled from deadspecimens found on the beach: Cystoseira compressa Gerloff &Nizamuddin; Scytosiphon lomentaria (Lyngbye) Link (Heterokon-tophyta, brown algae); Ulva compressa Linnaeus; Ulva rigida C.Agardh (Chlorophyta, green algae); Gracilaria bursa-pastoris (S.G.

1 Department of Marine Sciences, Polytechnic University of Marche, viaBrecce Bianche, Ancona, Italy.2 Department of Chemistry, Chemical Engineering and Materials,University of Aquila, via Vetoio, 67100 Aquila, Italy.

* Department of Marine Sciences, Polytechnic University of Marche, viaBrecce Bianche, 60131 Ancona, Italy; e-mail: c.pennesi@univpm.it.

January 2012 9

Gmelin) P.C. Silva; Porphyra leucosticta Thuret; Polysiphonia sp.(Rhodophyta, red algae); and Cymodocea nodosa (Magnoliophyta,marine seagrass). Seaweeds were collected from Portonovo(Conero Natural Park, Italy, Adriatic Sea) and Palombina Beach(Marche region coast, Italy, Adriatic Sea). Cymodocea nodosa wascollected from the beach in Gabicce (Marche region coast, Italy,Adriatic Sea). After collection, samples were washed with distilledwater and with HCl 0.1 mol/L. Acid washing (orbital rotary shakerat 250 rpm, room temperature, 10 g/L solid) allowed adsorbentprotonation, which eliminates interference of biosorption by othercations such as Na+, K+, Mg2+, Ca2+ (Veglio et al., 2003). Solidsamples were then dried at room temperature for three to fourdays until a stable weight was observed. Each macrophyte samplewas then shredded, and small parts of 1.0 to 1.2 cm were obtainedand stored.

Potentiometric Titrations. Macrophyte suspensions (5 g ofmacrophyte in 100 mL of deionised water) were titrated bystandard solutions of NaOH 0.1 N (basic branch) and HCl 0.1 N(acid branch). The pH of the suspension was measured aftereach addition of titrant (0.05 mL) by a pH-meter when stabilityhad been obtained (2 minutes).

Biosorption Tests. To rehydrate the sample before eachtest, 0.5 g of dried biomass were suspended in 100 mL of distilledwater (biomass concentration 5 g/L) for 30 minutes, at 150 rpm.No problem of slurry agitation occurred. Subsequently, a con-centrated solution of PbCl2 (1 g/L Pb, Carlo Erba Reagents CAS7758-95-4) was added according to experimental conditions.Aliquot amounts of solution were then periodically sampled forlead concentration determination. Samples were centrifuged(8000 g for 10 minutes) to eliminate any suspended matterbefore analytical determinations. The pH effect on equilibriumwas investigated through pH-edge tests, aimed at the de-termination of sorption isotherms at different equilibrium pH, asdescribed in detail elsewhere (Beolchini et al., 2003). In all thecases cited, the suspension pH was adjusted by HCl 0.1 N andcontrolled during the entire biosorption test. Control tests wereperformed without biomass and showed a constant leadconcentration in solution over time. This confirmed thatprecipitation did not take place and that no lead was releasedby the testing equipment. The sorption isotherms at constant pHof 5 were determined according to the subsequent additionmethod to save time and reagents, after preliminary batch testsaimed at the validation of this procedure (Pagnanelli et al., 2000).One hour of contact time proved to be satisfactory for reachingprocess equilibrium.

Analytical Determinations. Lead concentration in theliquid phase was determined by atomic absorption spectropho-tometry (Varian Spectra 2000). All samples were diluted withHNO3 at pH 2 and stored at 4 uC before the analysis. Most of thebiosorption tests were replicated twice and the coefficient ofvariation ranged from 2 to 5%.

Scanning Electron Microscopy with Energy-Dispersive X-Ray Microanalysis. After the proves, two different dehydratedsamples of C. compressa were mounted on aluminium stubs andcoated with gold (Polaron Range Sputter Coater). They wereimaged and analyzed using a scanning electron microscope(Philips SEM 515) equipped with an energy-dispersive x-raymicroanalysis system (EDS prism x-ray detector with IMIX-PCsystem), with a chamber pressure of 1026–1025 Torr, and anaccelerating voltage of 10 kV.

Results and DiscussionEffect of pH on Lead Biosorption by Cymodocea nodosa.

This part of the work was aimed at evaluating the influence ofpH on lead biosorption by Cymodocea nodosa. Figure 1 showslead sorption isotherms as determined for different values of theequilibrium pH.

It can be observed that Cymodocea nodosa sorption abilityincreases with pH in the investigated range, with the highestperformance (0.6 mmol/g) at pH 5 and the lowest at pH 3.3(0.3 mmol/g). This good lead sorption ability can be attributed tothe biochemical composition of the external layer constituents,such as cutin. In fact, carboxylic groups of this amorphoussubstance likely are responsible for the chemical and physicalbond with the lead cation (Sanchez et al., 1999). This hypothesisis also confirmed by Fourier transform infrared (FTIR)spectroscopy performed by other authors who investigated thesorption of marine algal biomass for a series of metal cations,including Pb (Sheng et al., 2004). They observed the sameincrease of sorption capacity with pH and characterized thebiosorbents using FT-IR spectroscopy. They correlated theenhancement of sorption with pH to the presence of weakcarboxylic acid groups (R–COO2) (apparent pKa in the range3.5–5.0) for alginate-rich algae; indeed, fucoidan-bearing sul-fonic acid groups (apparent pKa in the range 1–2.5) contributeslittle to biosorption. They showed that FTIR spectra wereminimally changed after metal sorption in the wavenumberrange representative of fucoidan (i.e., 1250 cm21). The bandsrepresentative of carboxylate groups, however, were significantlyshifted (by 200 cm21) after metal binding at <1630 cm21 and<1420 cm21, for asymmetrical and symmetrical stretchingbands, respectively. This suggests that most metal sorptionoccurs through chelation on carboxylics (bidentate complex)with contribution of alcoholic groups and amine groups toa lesser extent. Consequently, the decrease in lead binding in C.nodosa in conjunction with increasing ionic strength anddecreasing pH in solution likely is because of the effect ofproton competition, as already reported in the literature forother sorbents, considering that lead is present in the aqueoussolution as Pb2+ (Davis et al., 2003; Schiewer and Wong, 2000;Sheng et al., 2004). Furthermore, biosorption performances

Figure 1—Lead sorption isotherms at different pH (biomass 5 g/L, room temperature) for Cymodocea nodosa.

Pennesi et al.

10 Water Environment Research, Volume 84, Number 1

decreases with the extent of protonation of carboxyl groups. AtpH values lower than pKa, carboxylate groups are mainlyprotonated, resulting in a low lead uptake. At pH values higherthan pKa, more functional groups carry a negative charge andthe positively charged lead ions will be bound, increasing thelead uptake. The well-known Langmuir equation was first fittedto the experimental data (Langmuir, 1918):

q~qmax

:b:Ceq

1zb:Ceqð1Þ

Where

qmax 5 maximum adsorption (mmol/g) and b 5

affinity constant (L/mmol).

Figure 2 shows the estimated values for parameters qmax and b asa function of pH. Typically, an increase in qmax with pH can beobserved, as confirmation of the hypothesized competition betweenthe H3O+ and the lead cation. On the other hand, the parameterb shows a maximum of approximately 11 L/mmol for a pH in therange 4.3 to 4.5.

In conclusion, the results obtained suggested possible compe-tition between H3O+ and the lead cation. This hypothesis wasused as a basis for identification of an equilibrium model suitablefor the mathematical description of the whole dataset at thedifferent pHs. The simplest equation for this purpose is the ideal

competitive adsorption Langmuir model (ICA model), whichassumes homogenous sorbents and no interaction between Pb2+

and H3O+ (i.e., ideal sorption; Table 1) (Pagnanelli et al., 2005):

q~STOT

:KM:Ceq

1zKH:10{pHzKM

:Ceq

� � ð2Þ

Where

STOT 5 the concentration of active sites for biosorp-tion for both Pb2+ and H3O+ (meq/g) and KM

and KH are the affinity constants for lead andH3O+, respectively (L/meq).

The ascertained inadequacy of competitive Langmuir exten-sions in representing competition among ionic species guided themodeling toward introduction of surface heterogeneity and non-ideal sorption behavior (Koopal et al., 1994; Pagnanelli et al.,2003). Non-ideal competitive adsorption models (NICA models)have been specifically developed for metal sorption onto humicacids (Benedetti et al., 1995). The models account for both siteheterogeneity and interactions among ionic species that causenon-ideal sorption behavior (Pagnanelli et al., 2003). Pagnanelli etal. (2003) show the background theory and derivation of thesemathematical equations. These models are characterized byseveral adjustable parameters distinctly related to site heteroge-neity (affinity constants following Sips distribution) and the non-ideal sorption characteristics (interaction between H3O+ andPb2+) of each specific ionic component in solution (see Table 1).

q~STOT

~KM

:Ceq

� �a

~KM

:Ceq

� �az

~KH10{pH� �b

:

~KM

:Ceq

� �az

~KH10{pH� �b� �p

1z~KM

:Ceq

� �az

~KH10{pH

� �b� �pð3Þ

Where~KM and ~KH 5 median values of distribution for Pb2+ and

H3O+ affinity constants;a and b 5 ideal or non-ideal behavior of metal and

proton sorption because of negative orpositive cooperative phenomena orinteraction with other ionic species (n 5

1 ideal case; n ?1 non-ideal case); andp 5 intrinsic heterogeneity of the matrix.

Figure 2—Langmuir equation parameters as a function of pH(biomass 5 g/L, room temperature).

Table 1—Equilibrium competitive model performance (ICA = ideal competitive adsorption Langmiur model; NICA = non-idealcompetitive adsorption model).

Model ICA (Eq. 2) NICA (Eq. 3)

Estimated parameters STOT (meq/g) 1.2 6 0.2 STOT (meq/g) 1.29 6 0.06KH 9700 6 800 KH 15 400 6 200

a 0.58 6 0.06KM (L/meq) 5.4 6 0.9 KM (L/meq) 3.81 6 0.04

B 0.58 6 0.06p 3.1 6 0.6

R2 0.957 0.972Residual variance (meq/g)2 0.008 0.002Degrees of freedom 58 55

Pennesi et al.

January 2012 11

Both Eqs. 2 and 3 were fitted to experimental data bynonlinear regression techniques (Himmelblau, 1971). Table 1reports the estimated values for the adjustable parameterstogether with residual variances and degrees of freedom andFigure 3 shows experimental versus calculated data for the ICAmodel (a) and the NICA model (b). Both models provide a goodrepresentation of experimental data, which is confirmed both bythe low value estimated for the residual variance and highmultiple coefficient of determination, R2 (Table 1), and by thedistribution of points around the straight line (of equation qcalc

5 qexp) in the scatter diagrams in Figure 3. As expected, becauseof the higher number of adjustable parameters (6 versus 3), thepredictions by the NICA model denote an improvement incomparison with the ICA model (Figures 3a and 3b; modelresidual variances in Table 1). Nevertheless, this improvement inthe regression is offset by a higher complexity of the equilibriumequation, which has to be taken into account when used asa constitutive equation in dynamic models.

Effect of Macrophyte Structure on Lead Biosorption atConstant pH. This part of the work discusses the effect ofmacrophyte structure on lead biosorption equilibrium. Inparticular, seaweeds of different species were tested as leadbiosorbents. Preliminary experiments (data not reported here)showed that lead removal rates were high, with 90% of the totaladsorption taking place within 15 minutes for all macrophytes

and initial lead concentrations of 50 and 100 mg/L. Experimentswere performed at a constant pH of 5, chosen because leadbiosorption increases with pH and lead precipitation mightoccur at values greater than approximately 5.5. Previous researchhas established that when using microorganisms as biosorbents,an increase in biomass concentration reduces metal sorption pergram of biomass (Veglio et al., 1997). Basha et al. (2009)investigated the effect of biosorbent concentration on copperbiosorption by the brown seaweed Cystoseira indica in the range0.5 to 2.5 g/L and found an optimum for the specific uptake ata biosorbent dosage of 1 g/L. The focus of the present work,however, was not to assess the influence of sorbent concentra-tion. As a result, a value of 5 g/L was considered large enough toachieve substantial lead removal from the solution but not toohigh to have slurry agitation problems. (Application of biosorp-tion in a continuous stirred tank reactorsystem with relativelylarge fragments of biosorbent might ease solid/liquid separa-tion.) In fact, even if the specific uptake (mg Pb/g) might belower as biosorbent concentration increases, the absolute uptake(mg Pb) increases with the biosorbent.

Figure 4 shows equilibrium isotherms (lead solid concentra-tion, q, mmol/g, vs. lead liquid concentration at equilibrium, Ceq,mmol/L) as determined from experimental data at pH 5 androom temperature. First, the Langmuir equation (1) was fitted tothe experimental data. Table 2 shows the estimated values forthe parameters qmax and b for each marine macrophyte. Thereported data suggests that the seaweeds belonging to thephylum Rhodophyta (red algae) are the worst lead sorbents. Infact, maximum lead uptake was lower than 15 mg/g(0.068 mmol/g) in the case of both Porphyra and Polysiphoniaspecimens, and approximately 40 mg/g (0.19 mmol/g) forGracilaria biosorbent. The lack of sorption abilities of thePorphyra and Polysiphonia species might be related to thesimple structure of the thallus (i.e., the undifferentiatedvegetative tissue of the algae) compared to the Gracilariaspecies, which has a complex structure. Indeed, it can beassumed that there is a direct relationship between thecomplexity of its thallus and the adsorption of lead (Van denHoek et al., 1995). The two species belonging to the phylum

Figure 3—Calculated versus experimental data for data-fitting to:(A) Eq. 2, ideal competitive adsorption Langmuir model; and (B)Eq. 3, non-ideal competitive adorption model (biomass 5 g/L,room temperature) in Cymodocea nodosa.

Figure 4—Equilibrium lead sorption isotherm for the differentmarine macrophytes (pH 5, biomass 5 g/L, room temperature).

Pennesi et al.

12 Water Environment Research, Volume 84, Number 1

Chlorophyta (Ulva spp., green algae) showed a similar behavior,with a maximum uptake in the range 60 to 95 mg/g (0.30 to0.46 mmol/g) for both Ulva species. Because these macroalgaemay overpopulate, especially in closed zones, and may representa waste, their use as metal sorbents would be a potentialalternative for the valorization of such waste.. Both species ofbrown algae, which belong to the phylum Heterokontophyta(Cystoseira and Scitosyphon), appear to be promising metalsorbents. In fact, maximum lead uptake was estimated at220 mg/g (1.1 mmol/g) and 140 mg/g (0.68 mmol/g), forCystoseira and Scitosyphon, respectively. Previous studies alreadyhave found that other kinds of brown algae have the potential forbetter metal ion sorption compared with green and redseaweeds. The brown algae studied include Petalonia, Sargas-sum, Colpomenia, Padina, and other Cystoseira species (Cysto-seira indica, C. baccata and C. myrica) (Basha et al., 2008a,2008b, 2009; Khani et al., 2006; Lodeiro et al., 2006; Naddafi andSaeedi, 2009; Schiewer and Wong, 2000; Sheng et al., 2004). Thehighest value found in the literature for lead sorption wasapproximately 1.8 mmol/g for cross-linked species of brownalgae (Fucus and Ascophyllum) (Holan and Volesky, 1994).Moreover, the highest values for lead sorption by raw brownalgae (i.e., not pretreated) reported were 1.2 mmol/g forLaminaria japonica (Luo et al., 2006); 1.02 mmol/g for Fucusvesiculosus (Mata et al., 2008); and 0.98 for Fucus spiralis

(Romera et al, 2007). Consequently, the value found here forCystoseira compressa, 1.1 mmol/g at pH 5, confirms the resultsin the literature of 0.9 mmol/g at pH 4.5 observed for Cystoseirabaccata and confirms that the Cystoseira species are effectivelead sorbents (Lodeiro et al., 2006). This ability can be attributedto the biochemical composition of cell wall constituents, such asalginate polymer and fucoidan (sulfated muco-polysaccharides).In fact, previous studies have advocated that the biosorptionprocess is represented by the ion-exchange, which involves thecarboxyl group in the alginate polymer and sulfonic acid in thefucoidan (Davis et al., 2003). Therefore, it is assumed that thenumber of binding sites identified decreases in the orderCystoseira compressa . Scytosiphon lomentaria . Cymodoceanodosa . Ulva compressa . Ulva rigida . Gracilaria bursa-pastoris . Polysiphonia sp. . Porphyra leucosticta; or brownalgae . seagrasses . green algae . red algae. Biosorbentpotentiometric titration confirmed this trend. Figure 5 showsexamples of titration curves of C. compressa, U. rigida, and G.bursa-pastoris. The elaboration of titration data by means ofGran’s method (1950) allowed an estimate of the total number ofacidic sites potentially active for biosorption: 2.2 60.1, 1.5 60.1,1.2 60.2 meq/g for G. bursa-pastoris, U. rigida, and C.compressa, respectively. Equilibrium data have also beenelaborated by means of the Dubinin-Kaganer-Radushkevic(DKR) isotherm to gain further information regarding theprocess of adsorption. Such an isotherm is analogous toLangmuir type (Equation 1) but is more general because it doesnot assume a homogeneous surface or constant sorptionpotential (Ibrahim et al., 2010). The linearized DKR isothermequation can be written as:

ln q~ ln Xm{b e2 ð4Þ

Where

q 5 number of metal ion sorbed per unit weight ofadsorbent (mol/g),

Xm 5 saturation limit (mol/g),b 5 activity coefficient related to the mean sorption

energy, ande 5 Polanyi potential (kJ/mol), which is equal to:

e~RTln 1z1

Ceq

� �ð5Þ

WhereR 5 gas constant (0,008314 kJ/mol/K),T 5 temperature (298 K), and

Ceq (mol/L) 5 lead equilibrium concentration.

Figure 5—Titration curves of Cystoseira compressa (brownalgae), Ulva rigida (green algae), Gracilaria bursa-pastoris(red algae).

Table 2—Langmuir parameters for each marine macrophyte (Eq. 1).

Marine macrophyte qmax (mmol/g) b (L/mmol) R2

Brown algae Cystoseira compressa 1.1 6 0.1 5.4 6 0.4 0.978Scytosiphon lomentaria 0.68 6 0.05 48 6 4 0.981

Green algae Ulva rigida 0.30 6 0.02 4.4 6 0.3 0.989Ulva compressa 0.46 6 0.03 2.5 6 0.2 0.987

Red algae Gracilaria bursa-pastoris 0.19 6 0.01 5.0 6 0.4 0.989Porphyra leucosticta 0.068 6 0.005 33 6 3 0.981Polysiphonia sp. 0.068 6 0.005 6.8 6 0.5 0.979

Seagrass Cymodocea nodosa 0.69 6 0.04 7.1 6 0.6 0.976

Pennesi et al.

January 2012 13

The slope of the plot of ln q vs. e2 (Figure 6) gives b and theintercept yields the saturation limit. Table 3 shows the estimatedvalues for parameters together with regression coefficients R2.The estimation of parameter b allows an evaluation of the meansorption energy, E (kJ/mol), as follows:

E~ 2 bð Þ{1=2 ð6Þ

Sorption energies in the range 4 to 8 kJ/mol (Table 3) suggestthat lead biosorption by macrophytes is not only based on ionexchange (sorption energies in the range of 8 to 16 kJ/mol;Ibrahim et al., 2010) but also on other mechanisms, such ascomplexation.

In conclusion, because of their high number of binding sitesCystoseira compressa, Scytosiphon lomentaria, and Cymodoceanodosa are the most promising for biosorption applications.Moreover, the high metal-binding capacity of the brown algaecan be attributed to the morphological complexity of the thallus,which is high in the Cystoseira and low in Porphyra where thethallus consists of only one layer of cells (Graham and Wilcox,2000). Elemental distributions in the thallus of Cystoseiracompressa was determined using scanning electron microscopycoupled with energy dispersive x-ray microanalysis (Figures 7and 8). This type of detector allows a user to analyze themolecular composition of a sample. This analysis also confirmsthe other data obtained in this study. Indeed, the EDS profilescollected on the thallus after the treatment clearly show anenrichment in Pb compared to the untreated thallus (Figure 7).Moreover, a comparison between the two SEM-images of thethallus of C. compressa, before (Figure 8A) and after (Figure 8B)treatment shows a change in cell morphology after contact withlead. The heavy metal is even more concentrated in the outerparts of the thallus, suggesting that it is associated to the cellwall.

ConclusionsThis work deals with lead sorption by marine macrophytes.

This results of the research show that the equilibrium pH hada strong influence on the adsorption process, pH 5 being theoptimum for uptake, in the investigated range. Typically, anincrease in lead biosoption with pH was observed, as confirma-tion of the hypothesized competition between the H3O+ and thelead cation. Equilibrium data for lead sorption by the seagrassCymodocea nodosa at different pHs were successfully fitted tocompetitive equilibrium models (i.e., ICA and NICA). Thesemodels can be useful not only to optimize operating conditionsbut also as a constitutive equation in dynamic models forcontinuous processes. Both models provide a good representa-tion of experimental data; the NICA model, however, showeda better fitting of the data. In conclusion, adsorption behavior

Figure 6—Dubinin-Kaganer-Radushkevic (DKR) plots for leadadsorption onto different marine macrophytes (pH 5, biomass5 g/L, room temperature).

Table 3—Dubinin-Kaganer-Radushkevic (DKR) isotherm parameters for each marine macrophyte (Eqs. 4 and 5).

Marine macrophyte Xm (mmol/g) b (mol2/kJ2) Sorption energy (kJ/mol) R 2

Brown algae Cystoseira compressa 980 6 90 0.027 6 0.003 4.3 0.911Scytosiphon lomentaria 730 6 30 0.0094 6 0.0003 7.3 0.991

Green algae Ulva rigida 230 6 30 0.015 6 0.002 5.6 0.902Red algae Gracilaria bursa-pastoris 180 6 10 0.032 6 0.002 3.9 0.979

Porphyra leucosticta 74 6 6 0.011 6 0.002 6.5 0.941

Figure 7—A comparison between energy-dispersive x-rayspectrums of thallus of Cystoseira compressa before (A) andafter (B) the treatment with solution of Pb (5 g/L).

Pennesi et al.

14 Water Environment Research, Volume 84, Number 1

resulted to be non-ideal according to both biochemistry(complexity of the structure of C. nodosa external layer) andstatistics (better data fitting). The brown marine algae Cystoseiracompressa showed promising lead sorption ability, comparablewith the highest values available in the literature for rawbiomass. Furthermore, green algae (Ulva spp.) and the seagrassCymodocea nodosa also proved to be effective sorbents,especially if compared with low-cost sorbents such as naturalzeolites (0.08 mmol/g) and powdered activated carbons(0.10 mmol/g) (Matheickal and Yu, 1999). This study alsoconfirmed the influence of macrophyte structure on leadbiosorption. The lead binding ability decreased in the orderbrown algae . seagrasses . green algae . red algae.

Acknowledgements

The authors are grateful to Professor Francesco Veglio for hishelp in the experimental design. Special thanks are given to L.Gobbi, Ph.D., and to Marcello Centofanti for their cooperationin the analytical determinations.

Manuscript submitted for publication October 7, 2010; revisedmanuscript submitted February 28, 2011; accepted for publica-tion April 4, 2011.

ReferencesBasha, S.; Murthy, Z. V. P.; Jha, B. (2008a) Biosorption of Hexavalent

Chromium by Chemically Modified Seaweed Cystoseira indica.Chem. Eng. J., 137 (3), 480–488.

Basha, S.; Murthy, Z. V. P.; Jha, B. (2008b) Isotherm modeling forBiosorption of Cu(II) and Ni(II) from Wastewater onto BrownSeaweed Cystoseira indica. AIChE J., 54 (12), 3291–3302.

Basha, S.; Murthy, Z. V. P.; Jha, B. (2009) Removal of Cu(II) and Ni(II)from Industrial Effluents by Brown Seaweed Cystoseira indica. Ind.Eng. Chem. Res., 48 (2), 961–975.

Benavente, J.; Ramos-Barrado, J. R.; Heredia, A. (1998) A Study of theElectrical Behaviour of Isolated Tomato Cuticular Membranes andCutin By Impedance Spectroscopy Measurements. Colloids Surf., A,140, 333–338.

Beolchini, F.; Pagnanelli, F.; Reverberi A; Veglio F. (2003) CopperBiosorption onto Rhizopus oligosporus: pH-Edge Tests and Relatedkinetic and Equilibrium Modelling. Ind. Eng. Chem. Res., 42 (20),4881–4887.

Cengiz, S.; Cavas. L. (2008) Removal of Methylene Blue by InvasiveMarine Seaweed: Caulerpa racemosa var. cylindracea. Bioresour.Technol., 99, 2357–2363.

Davis, T. A.; Volesky, B.; Gucci, A. (2003) A Review of the Biochemistryof Heavy Metal Biosorption by Brown Algae. Water Res., 37, 4311–4330.

Ghimire, K. N.; Inoue, K.; Ohto, K.; Hayashida, T. (2008) AdsorptionStudy Of Metal Ions Onto Crosslinked Seaweed Laminariajaponica. Bioresour. Technol., 99, 32–37.

Graham, L. E.; Wilcox, L. W. (2000) Algae. Prentice-Hall: Upper SaddleRiver, New Jersey.

Gran, G. (1950) Determination of the Equivalent Point in PreviousTermpotentiometric Titrations, Next Term. Acta Chem. Scand., 4,559–577.

Himmelblau, D. M. (1971) Process Analysis by Statistical Methods. JohnWiley and Sons, Inc.: New York.

Holan, Z. R.; Volesky, B. (1994) Biosorption of Lead and Nickel byBiomass of Marine Algae. Biotechnol. Bioeng., 43, 1001–1009.

Ibrahim, H. S.; Jamil, T. S.; Hegazy, E. Z. (2010) Application of ZeolitePrepared from Egyptian Kaolin for the Removal of Heavy Metals: II.Isotherm Models. J. Hazard. Mater., 182, 842–847.

Khani, M. H.; Keshtkar, A. R.; Meysami, B.; Zarea, M. F.; Jalali, R. (2006)Biosorption of Uranium from Aqueous Solutions By NonlivingBiomass of Marine Algae Cystoseira indica. Electron. J. Biotechnol.,9 (2), 100–106.

Klimmek, S.; Stan, H. J.; Wilke, A.; Bunke, G.; Buchholz, R. (2001)Comparative Analysis of the Biosorption of Cadmium, Lead, Nickeland Zinc by Algae. Environ. Sci. Technol., 35, 4283–4288.

Koopal, L. K.; Benedetti, M. F. (1994) Analytical Isotherm Equations forMulticomponent Adsorption to Heterogenous Surfaces. J. ColloidInterface Sci., 166, 51–60.

Langmuir, I. (1918) The Adsorption of Gases on Plane Surfaces of Glass,Mica and Platinum. J. Am. Chem. Soc., 40, 1361–1402.

Lee, H. S.; Volesky, B. (1997) Interaction of Light Metals and Protonswith Seaweed Biosorbent. Water Res., 31 (12), 3082–3088.

Lodeiro, P.; Barriada, J. L.; Herrero, R.; Sastre de Vicente, M. E. (2006)The Marine Macroalga Cystoseira baccata as Biosorbent forCadmium(II) and Lead(II) Removal: Kinetic and EquilibriumStudies. Environ. Pollut., 142 (2), 264–273.

Luo, F.; Liu, Y.; Li, X.; Xuan, Z.; Ma, J. (2006) Biosorption of Lead Ion byChemically Modified Biomass of Marine Brown Algae Laminariajaponica. Chemosphere, 64 (7), 1122–1127.

Mata, Y. N.; Blazquez, M. L.; Ballester, A.; Gonzalez, F.; Munoz, J.A. (2008)Characterization of the Biosorption of Cadmium, Lead and Copperwith the Brown Alga Fucus vesiculosus. J. Hazard. Mater., 158, 2–323.

Matheickal, J. T.; Yu., Q., 1999. Biosorption of Lead(II) and Copper(II)from Aqueous Solutions by Pre-Treated Biomass of AustralianMarine Algae. Bioresource Technology, 69 (3), 223–229.

Figure 8—Scanning electron microscope images of the thallusdehydrated of Cystoseira compressa, before (A) and after (B) thetreatment with lead.

Pennesi et al.

January 2012 15

Murphy, V.; Hughes, H.; McLoughlin, P. (2008) Comparative study ofChromium Biosorption by Red, Green and Brown SeaweedBiomass. Chemosphere, 70, 1128–1134.

Naddafi, K.; Saeedi, R. (2009) Biosorption of Copper(II) from AqueousSolutions by Brown Macroalga Cystoseira myrica Biomass. Environ.Eng. Sci., 26 (5), 1009–1015.

Pagnanelli, F.; Esposito, A.; Toro, L.; Veglio, F. (2003) Metal Speciation andpH effect on Pb, Cu, Zn and Cd Biosorption onto Sphaerotilus na-tans: Langmuir-Type Empirical Model. Water Res., 37 (3), 627–633.

Pagnanelli, F.; Petrangeli Papini, M.; Trifoni, M.; Toro, L.; Veglio, F.(2000) Biosorption of Metal Ions on Arthrobacter sp.: BiomassCharacterization and Biosorption Modeling. Environ. Sci. Technol.,34, 2773–2778.

Pagnanelli, F.; Mainelli, S.; De Angelis, S.; Toro, L. (2005) Biosorption ofProtons and Heavy Metals onto Olive Pomace: Modelling ofCompetition Effects. Water Res., 39 (8), 1639–1651.

Romera, E.; Gonzalez, F.; Ballester, A.; Blazquez, M. L.; Munoz, J. A(2007) Comparative Study of Biosorption of Heavy Metals UsingDifferent Types of Algae. Bioresour. Technol., 98 (17), 3344–3353.

Sanchez, A.; Ballester, A.; Blazquez, M.L.; Gonzalez, F.; Munoz, J.;Hammaini, A. (1999) Biosorption of Copper and Zinc byCymodocea nodosa. FEMS Microbiol. Rev., 23, 527–536.

Schiewer, S.; Volesky, B. (2000) Biosorption by Marine Algae. InRemediation, Valdes, J. J., Ed.; Kluwer Academic PublishersDordrecht, Netherlands.

Schiewer, S.; Wong, M. H. (2000) Ionic Strength Effects in Biosorption ofMetals by Marine Algae. Chemosphere, 41, 271–282.

Sheng, P. X.; Ting, Y. P.; Paul Chen, J.; Hong L. (2004) Sorption ofLead, Copper, Cadmium, Zinc, and Nickel by Marine AlgalBiomass: Characterization of Biosorptive Capacity and In-vestigation of Mechanisms. J. Colloid Interface Sci., 275, 131–141.

Tien, C. J. (2002) Biosorption of metal ions by freshwater algae withdifferent surface characteristics. Process Biochem., 38, 605–613.

Van den Hoek, C.; Mann, D. G.; Jahns, H. M. (1995) Algae. AnIntroduction to Phycology. Cambridge University Press: Cambridge,United Kingdom.

Veglio, F.; Beolchini, F. (1997) Removal of Metals by Biosorption: AReview. Hydrometallurgy, 44, 301–319.

Veglio, F.; Beolchini, F.; Gasbarro, A. (1997) Biosorption of Toxic Metals:An Equilibrium Study Using Free Cells of Arthrobacter sp. ProcessBiochem., 32 (2), 99–105.

Veglio, F.; Esposito, A.; Reverberi, A. P. (2003) Standardisation of HeavyMetal Biosorption Tests: Equilibrium and Modelling Study. ProcessBiochem., 38 (6), 953–961.

Vijayaraghavan, K.; Yun, Y -S. (2008) Biosorption of C.I. Reactive Black 5from Aqueous Solution Using Acid-Treated Biomass of BrownSeaweed Laminaria sp. Dyes Pigm., 76, 726–732.

Volesky, B. (1990) Removal and Recovery of Heavy Metals byBiosorption. In Biosorption of Heavy Metals, Volesky, B., Ed.; CRCPress: Boca Raton Florida.

Yun, Y. S.; Park, D.; Park, J. M.; Volesky, B. (2001) Biosorption ofTrivalent Chromium on the Brown Seaweed Biomass. Environ. Sci.Technol., 35, 4353–4358.

Pennesi et al.

16 Water Environment Research, Volume 84, Number 1