Int. J. Miner. Process. 62 2001.

111120
www.elsevier.nlrlocaterijminpro

Biosorption of metals onto plant biomass: exchange

adsorption or surface precipitation?
Ivo A.H. Schneider a , Jorge Rubio b, Ross W. Smith c,)
a
Ciil Engineering Department, Uniersity of Paso Fundo, Paso Fundo RS, Brazil
Department of Mining Engineeringr PPGEMM, Federal Uniersity of Rio Grande do Sul,
Porto Alegre RS, Brazil
Department of Chemical and Metallurgical Engineering, Uniersity of Neada-Reno, Reno, NV 89557 USA
b

Received 15 August 1999; accepted 17 July 2000

Abstract
Heavy metal ions readily adsorb onto the nonliving biomass of many aquaphytes. Further, in
many cases the metal ions can be readily desorbed from the biomass by use of a suitable eluting
agent. It has been shown in certain cases, at least, that the biomass can be subjected to a number
of loading and elution cycles without the biomass losing its adsorption capacity. It has been
widely reported that the adsorption is through a specific ion exchange mechanism and a number of
researchers have shown experimental evidence supporting such a mechanism. However, there is
also evidence that the adsorption is through simple surface precipitation of metal hydroxide
species. The present study examines some of the existing data on adsorption of metal ions onto
aquaphyte biomass and attempts to evaluate which mechanism is the more likely. q 2001 Elsevier
Science B.V. All rights reserved.
Keywords: aquaphyte; adsorption; precipitation; heavy metals

1. Introduction
Heavy metal ions sorb onto many solid surfaces including the surfaces of living and
dead microorganisms and higher plants. A characteristic of the sorption of heavy metal
ions onto surfaces, both biotic and abiotic surfaces, is that at a set bulk solution heavy
metal concentration the sorption is greatest at a pH value that is just slightly more acidic
)

Corresponding author. Fax: q1-775-327-5059.

E-mail addresses: ivoandre@fear.upf.br I.A.H. Schneider., jrubio@vortex.ufrgs.br J. Rubio.,
smithrw@scs.unr.edu R.W. Smith..
0301-7516r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 1 - 7 5 1 6 0 0 . 0 0 0 4 7 - 8

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I.A.H. Schneider et al.r Int. J. Miner. Process. 62 (2001) 111120

than the pH at which there is bulk precipitation of the metal hydroxide. As pH is further
raised, once the bulk solubility limit is reached, the sorption is greatly reduced because
the metal ion is removed from solution by the bulk precipitation.
It has long been reported that the sorption of heavy metal ions onto algae, bacteria
and higher plants is through a specific ion exchange mechanism. The sorption is thought
to involve the replacement of protons, alkali, alkaline earth, or other cations by the
heavy metal ions. Evidence presented by various researchers includes evidence that for
each heavy metal ion sorbing an equivalent of protons andror other metal ions appear in
solution Crist et al., 1991: Schneider et al., 1999.. Further evidence is the fit, or
approximate fit, of the sorption data obtained to the Langmuir isotherm Wang, 1995;
Schneider, 1995; Wang et al., 1998, Schneider et al., 1999.. The former is apparent
direct evidence that a replacement phenomenon is taking place. The Langmuir fit is
considered to be evidence that sorption stops at one monolayer, consistent with specific
and strong sorption onto specific sites. Because the exchange reaction between surface
sites and previously adsorbed ions is of only a monolayer or less, there is an
accumulation of matter at the solidsolution interface without the creation of a three-dimensional structure. Thus, the phenomenon is adsorption.
Evidence against such a mechanism is the often reported very low sorption activation
energy, which is not consistent with strong sorption onto specific sites, the extreme
rapidity with which the sorption takes place and the very rapid and easy and rapid
desorption Schneider, 1995; Wang et al., 1998, Schneider et al., 1999.. In addition, it
can often be observed that sorption of heavy metal ions onto biomass is partly in patches
Golab et al., 1991; Golab and Smith, 1992; Bauer, 1999..
An alternate sorption mechanism is the surface precipitation or condensation of heavy
metal hydroxides onto the biosurfaces. Such precipitation is possible if there is an
accumulation of the heavy metals within the diffuse part of the electrical double layer.
The accumulation will take place if there is a net negative charge on the solid surface.
Thus, although the concentration of the metal ion in solution may be much less than the
solubility limit with respect to metal hydroxide and oxide solids, the solubility limit near
the solid surfaces is exceeded and precipitation onto the solid surface takes place.
The concentration of heavy metal ions within the electrical double layer can be
roughly calculated by use of the Boltzmann equation Gaudin and Fuerstenau, 1955.:
Ci surf . s Ci bulk . exp yzFfdrRT .

1.

where Ci surf. s concentration of species i at the surface; Ci bulk. s concentration of

species i in the bulk of the solution; z s formal charge on the cation; F s Faraday
constant; fd s potential at the Stern plane; R s gas constant; T s absolute temperature.
In the present paper an attempt is made to evaluate the magnitude of the effect of the
concentration of CuII. within the electrical double layer and determine if the concentration is sufficient to account for the sorption of CuII. onto a macrophyte.
2. Results and discussion
Fig. 1 shows a log concentration diagram, adapted from Baes and Mesmer 1986. for

Cu II. in equilibrium with solid CuOH. 2 . It can be seen at pH values more acidic than

I.A.H. Schneider et al.r Int. J. Miner. Process. 62 (2001) 111120

113

Fig. 1. Logarithm concentration diagram for CuII. in equilibrium with solid CuOH. 2 .

pH 7 that the solubility increases rapidly with decrease in pH and that the solubility is
about 10y3 .36 molrL at pH 6.0. If a 1.0 = 10y4 molrl CuII. solution is considered, the
bulk solubility limit is reached at about pH 6.3 Fig. 2 from Schneider 1995., based on
data of Baes and Mesmer 1986., shows CuII. species distribution for a total CuII.
concentration of 1 = 10y4 molrL. Fig. 3 from Schneider et al. 1995. shows the
sorption of CuII. onto Potomogenten luscens as a function of pH. The curves of this
figure should be compared to the curves of Figs. 1 and 2. It is noted that maximum
sorption of CuII. occurs at a pH value slightly more acidic than the pH of bulk
precipitation of CuOH. 2 .

Fig. 2. Relative concentration of CuII. species in a system containing 1=10y4 molrl CuII.; from Schneider
1995..

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I.A.H. Schneider et al.r Int. J. Miner. Process. 62 (2001) 111120

Fig. 3. Final concentration of CuII. in solution as a function of pH; total CuII. in the system s1=10y4
molrl CuII.; from Schneider 1995..

Fig. 4 from Schneider 1995. shows the zeta potential z . of P. luscens as a function
of pH. Using z data from this figure and substituting z for fd in the Boltzmann
equation, it is possible to approximately solve the Boltzmann for the concentration of
CuII. within the electrical double for the biomass at different pH values. The substitution is necessary since fd is an inner potential and is not measurable while z is an
outer, measurable, potential. In the calculation, it should be kept in mind that at all pH
values more basic than the isoelectric point of the plant biomass, fd will be more
negative than z and, thus, the calculation will always underestimate the concentration of
CuII. within the electrical double layer.
It can be noted from Fig. 1 that the pH value of bulk solution precipitation of
CuOH. 2 for a CuII. solution containing 1.0 = 10y4 molrl CuII. is at about pH 6.3.
This means that at pH values more basic than this pH, there will be a precipitate of
CuOH. 2 present in the system. From Fig. 4 it is seen that the zeta potential values for

Fig. 4. Zeta potential of P. luscens as a function of pH; 1=10y3 molrl NaNO 3 added for ionic strength
control; from Schneider 1995..

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115

Table 1
Concentration of CuII. within the electrical double layer at selected pH values
pH

Concentration of CuII. within double

layer molrl; total bulk concentration
CuII. s1=10y4 molrl.

Maximum concentration of soluble

CuII. in equilibrium with solid
CuOH. 2 molrl.

4.0
5.0
6.0
6.3
7.0

10y1.87
10y1 .38
10y1 .03
10y0 .86 bulk solubility limit reached.
10y1 .4 bulk solubility limit exceeded.

10 0.64
10y1.36
10y3.36
10y4
10y5.36

the P. luscens biomass at pH 4, 5, 6 and 7 are approximately y60, y75, y85 and
y100 mV, respectively. For a total bulk CuII. concentration of 1.0 = 10y4 molrl and
using the Boltzmann equation the concentrations of CuII. within the diffuse part of the
double layer can be roughly calculated. Table 1 shows the amount of CuII. in the
electrical double layer as a function of pH. Thus, it can be seen that at all pH values
more acidic than pH 6.3, the solubility limit of CuII. is exceeded and there should be
precipitation of CuOH. 2 within the double layer. Assuming different values for the total
concentration of CuII. in a system, the pH value at which the double layer concentration of CuII. approximately equals the solubility limit in the bulk solution can be
determined for these total concentrations of CuII.. This data is presented in Table 2 for
CuII. concentrations from 1 = 10y8 to 1 = 10y4 molrl.
Recent work by Schneider 1995. shows that the sorption of CuII., NiII., and ZnII.
onto P. luscens, Salinia herzogii, and Eichhornia crassipes can be fitted to a
Langmuir isotherm. Furthermore, the sorption of these ions appears to involve an ion
exchange mechanism whereby either the ions exchange with protons or with other
cations in equivalent amounts Wang, 1995; Wang et al., 1997; Schneider et al., 1999..
It was deduced that the surface group responsible for the exchange was primarily the
carboxylate group. In addition, this work confirmed previous work that the isoelectric
point iep. of all three macrophytes is at about pH 2.0. The p K a of the carboxylate
groups in fatty acids is at pH 4.7, but there is evidence that it is at a more acidic value in

Table 2
The pH value at which the concentration of CuII.aq. species within the double layer equals the maximum
concentration of CuII.aq. species in the bulk solution as a function of total CuII. in the system
Total concentration of CuII. in system
molrl.

The pH at which the concentration of

CuII.aq. within the double layer equals
the maximum concentration in
the bulk of the solution

1=10y4
1=10y5
1=10y6
1=10y7
1=10y8

5.0
5.4
5.8
6.3
6.8

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116

other structures Smith, 1989.. From the iep data, assuming that there is no inherent
space charge in the macrophytes, it appears that the p K a of the macrophytes is near pH
2.0. Thus, since the number of positive and negative sites on the macrophytes are equal
at the iep, the carboxylate groups must be primarily ionized at pH values only slightly
more basic than pH 2. In the absence of foreign cations, hydrogen ions, thus, at pH
values more basic than the iep must be primarily located in the diffuse part of the double
layer. Any exchange by introduced cations must be with double layer protons and the
observed experimental exchange is primarily due to coulombic interaction between the
cations and the charged surface. Schneider 1995. observed that, although there was
some loss of CuII. sorptive capacity of a P. luscens biomass after several loading and
elution cycles using a O.5% solution of HCl as eluant, the sorptive capacity remained
essentially unchanged for up to 100 loading and elution cycles. However, after subjecting the plant biomass to 50 cycles, analysis of the biomass indicated that there remained
a substantial amount of CuII. on the biomass. The data are shown in Table 3. This
CuII. was only partially removed with 5% HCl treatment. Thus, there must be both
CuII. adsorption onto specific sites and non-specific, reversible, sorption through
coulombic interaction between the CuII. ions and the negative biomass surface.
Electrostatic models for exchange reactions at humicwater interfaces Hummel,
1997., at hydrous ferric hydroxide surfaces Dzombak and Morel, 1990., and at
geological solids surfaces Banwart, 1997. have been suggested. In such cases, the
model may include surface precipitation. The model for surface precipitation generally
includes an initial, rapid, adsorption mechanism followed by a slower surface precipitation. Thus, there is adsorption on the surface with a surface precipitation layer covering
the adsorbed layer. A rough sketch of the conceptual model is shown in Fig. 5 based on
figures from Banwart 1997. and Dzombak and Morel 1990..
In addition to the various models, there is considerable question about the true
surface areas of dried plant biomass and soil organic matter SOM. since various surface
areas can be measured depending on measurement technique and there is the possibility
of the materials swelling upon reaction with water. Table 4 shows some measured values
of selected materials.
Immediately evident from the table is that BET surface area measurements using N2
determined at 77 K, the vaporization temperature of N2 , are much less than those

Table 3
Amount of CuII. remaining in the biomass after 50 loading and elution cycles and after a final elution cycle
with both 0.5% and 5% HCl solutions

E. cressipes
P. lucens

Cu concentration natural dead

biomass before sorption
and elution cycles
mg Curkg biomass.

Cu concentration biomass
after 50 cycles of loading
and elution using 0.5%
HCl solution as eluant

Cu concentration biomass
after 50 cycles of loading
and elution using 0.5%
HCl solution as eluant
followed by a cycle using
5% HCl as eluant

46
19

384
327

187
129

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117

Fig. 5. Representation of the model from Dzombak and Morel 1990. representing the relative contribution of
adsorption and surface precipitation to metal sorption.

determined using other methods. These much larger surface areas of materials such as
soil organic matter SOM. as measured by ethylene glycol EG. or ethylene glycol

Table 4
Selected values for the specific surface areas of porous solids measured by different techniques
Adsorbent
E. crassipes
roots.
E. crassipes
roots.
E. crassipes
roots.
E. crassipes
aerial parts.
E. crassipes
roots.
E. crassipes
aerial parts.
Salinia sp.
Salinia sp.
P. lucens
Soil organic
matter SOM.
SOM
SOM

Pretreatment

0.1 M H 2 SO4

Adsorbate

Temperature Surface area Reference

K.
M 2 rg.

N2

77

7.4

Wang 1995.

N2

77

6. 7

Wang 1995.

)150

Schneider et al. 1995.

N2 slow drift 77
toward
equilibrium.
N2 slow drift 77
toward
equilibrium.
Methylene blue ; 298

; 280

This study

243

Schneider et al. 1995.

Methylene blue ; 298

223

Schneider et al. 1995.

; 298
; 298

274
278

Schneider 1995.
Ribeiro et al. 1998.

; 298
77

415
0.891.1

273

94174

Schneider 1995.
De Jonge and MittlemeijerHazeleger 1996.
De Jonge and MittlemeijerHazeleger 1996.
Bower and Gschwend 1952.

Methylene blue
Hydrophobic
Methylene blue
surface removed
Methylene blue
N2
CO 2

Ethylene glycol 298"2

560800

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I.A.H. Schneider et al.r Int. J. Miner. Process. 62 (2001) 111120

monethyl ether EGME. uptake Heilman et al., 1965., compared to areas measured by
the BET method, has led to the suggestion that the larger surface areas are not real. For
example, Chiou et al. 1990, 1992. have argued that to consider that surface areas
measured by fluids such as EG or EGME onto SOM would require the existence of an
Ainner surfaceB that is accessible to these fluids but somehow excludes smaller
molecules such as N2 . Their suggested alternate mechanisms involve the expansion of
the clays or SOM by the fluids creating new surface and, importantly, the solubility of
the AadsorbateB in the AadsorbentB. Pennell and Rao 1992. take strong exception to this
interpretation of EG and EGME sorption and propose that SOM, for example, behaves
as a three dimensional system in a semi-structural framework. Further, they note the
very high ion exchange capacity for SOM is not consistent with the model of Chiou et
al. 1990.. Although De Jonge and Mittlemeijer-Hazeleger 1996. believe that EG and
EGME give unrealistically high values for the surface areas of SOM, BET surface areas
using N2 at 77 K give values that only represent an Aexternal surfaceB and exclude
micropores and inner surfaces. As evidence, their work measuring the surface areas of
SOMs showed that N2 adsorption at 77 K gave values between 0.89 and 4.94 m2rg and
that CO 2 adsorption at 273 K gave values between 94 and 174 m2rg. Furthermore, the
work of Rodriguez-Reinoso et al. 1982, 1984. indicates that CO 2 adsorption at 195 and
273 K and N2 adsorption at 90 K yield much greater surface areas of activated carbons
than N2 adsorption at 77 K. However, a slow drift was noted in the latter system. Then,
if the system was allowed to drift for 6 weeks, apparent equilibrium was reached and the
surface area values were comparable to those measured by CO 2 adsorption and N2
adsorption at 90 K. The conclusion De Jonge and Mittlemeijer-Hazeleger, 1996. is that
N2 adsorption at 77 K will not measure pores with restrictions less than 0.5 nm unless
long adsorption times weeks. are considered. Since the surface area of SOMs estimated
by microscopic examination is about 0.05 m2rg, they also believe that the surface areas
measured by fast N2 adsorption at 77 K includes pores between 0.5 and 2 nm where
capillary condensation can take place.. Schneider et al. 1995. attempted to measure the
surface area of various parts of E. crassipes. It was found that it initially appeared that
the surface areas were between 2 and 5 m2rg. However, a slow drift was noted in the
systems and after several days measured areas between 150 and 280 m2rg. It was still
not certain that equilibrium had been reached. Ruthven and Kaul 1993. have suggested
that in such systems the rate of diffusion into pores of porous solids is governed
primarily by the rotational freedom of the diffusing molecule rather than the energy
barrier associated with the penetration of pore restrictions. Thus, metal ions can either be
present on the surface of the biomass or can go into expanded pores. In this latter case,
the metal ions should be difficult to desorb.
Furthermore, regardless of mechanisms involved, displacement of protons from the
anchored layer and diffuse layer by metal cations will take place. In addition, the
replacement of one species of metal ion by another species should take place both at and
near the biomass surface. Although the data can usually be fitted to a Langmuir
isotherm, careful inspection of the data often shows some evidence, at low equilibrium
concentrations of the metal ion, of a stronger sorption mechanism also taking place
Schneider et al. 1995; Wang, 1995.. For HgII. sorption onto P. natans biomass
electron microscopy evidence shows that, although HgII. was present over the entire

I.A.H. Schneider et al.r Int. J. Miner. Process. 62 (2001) 111120

119

biomass surface, there were patches where definite multilayer sorption occurred Bauer,
1999.. Also, in the case of sorption of PbII. onto algae and bacteria dead biomass
Golab et al., 1991; Golab and Smith, 1992., there is physical evidence from electron
microscopic examination of the microorganisms that the PbII. has sorbed in discrete
patches onto the biomass. This suggests that not only is the sorption at least in part a
precipitation phenomenon, but also that there may be reactive sites or patches on the
biomass surface. A similar sorption was observed with uranyl sorption onto a Streptomyces sp., although the evidence is not quite as convincing as with PbII..
In attempting to distinguish between adsorption and surface precipitation in the
accumulation of metal ions onto solid surfaces, Sposito 1986. deduced that it is not
possible to differentiate between the two phenomena based solely on sorption data.
Rather, determination of the mechanism must be achieved through close spectroscopic
determination of the molecular structure of the sorbed layer.
Considering the data and analysis presented in this paper, it is suggested that both
mechanisms can be thought of as taking place in sorption of heavy metal ions such as
CuII. onto plant biomass surfaces.

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