.

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
b
Department of Mining EngineeringrPPGEMM, Federal Uniersity of Rio Grande do Sul,
Porto Alegre RS, Brazil
c
Department of Chemical and Metallurgical Engineering, Uniersity of Neada-Reno, Reno, NV 89557 USA
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. q2001 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 q2001 Elsevier Science B.V. All rights reserved.
.
PII: S0301- 7516 00 00047- 8
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 112
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-di-
mensional 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 :
C surf sC bulk exp yzF rRT 1 . . . .
i i fd
. .
where C surf sconcentration of species i at the surface; C bulk sconcentration of
i i
species i in the bulk of the solution; zsformal charge on the cation; FsFaraday
constant; f spotential at the Stern plane; Rsgas constant; Tsabsolute temperature.
d
In the present paper an attempt is made to evaluate the magnitude of the effect of the
.
concentration of Cu II within the electrical double layer and determine if the concentra-
.
tion is sufficient to account for the sorption of Cu II 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 Cu OH . It can be seen at pH values more acidic than
2
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 113
. .
Fig. 1. Logarithm concentration diagram for Cu II in equilibrium with solid Cu OH .
2
pH 7 that the solubility increases rapidly with decrease in pH and that the solubility is
y3.36 y4
.
about 10 molrL at pH 6.0. If a 1.0=10 molrl Cu II 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 Cu II species distribution for a total Cu II
y4
.
concentration of 1=10 molrL. Fig. 3 from Schneider et al. 1995 shows the
.
sorption of Cu II 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 Cu II occurs at a pH value slightly more acidic than the pH of bulk
.
precipitation of Cu OH .
2
.
y4
.
Fig. 2. Relative concentration of Cu II species in a system containing 1=10 molrl Cu II ; from Schneider
.
1995 .
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 114
. .
y4
Fig. 3. Final concentration of Cu II in solution as a function of pH; total Cu II in the systems1=10
. .
molrl Cu II ; 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 f in the Boltzmann
d
equation, it is possible to approximately solve the Boltzmann for the concentration of
.
Cu II within the electrical double for the biomass at different pH values. The substitu-
tion is necessary since f is an inner potential and is not measurable while z is an
d
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, f will be more
d
negative than z and, thus, the calculation will always underestimate the concentration of
.
Cu II within the electrical double layer.
It can be noted from Fig. 1 that the pH value of bulk solution precipitation of
. .
y4
.
Cu OH for a Cu II solution containing 1.0=10 molrl Cu II is at about pH 6.3.
2
This means that at pH values more basic than this pH, there will be a precipitate of
.
Cu OH present in the system. From Fig. 4 it is seen that the zeta potential values for
2
Fig. 4. Zeta potential of P. luscens as a function of pH; 1=10
y3
molrl NaNO added for ionic strength
3
.
control; from Schneider 1995 .
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 115
Table 1
.
Concentration of Cu II within the electrical double layer at selected pH values
.
pH Concentration of Cu II within double Maximum concentration of soluble
.
layer molrl; total bulk concentration Cu II in equilibrium with solid
y4
. . . .
Cu II s1=10 molrl Cu OH molrl
2
y1.87 0.64
4.0 10 10
y1.38 y1.36
5.0 10 10
y1.03 y3.36
6.0 10 10
y0.86 y4
.
6.3 10 bulk solubility limit reached 10
y1.4 y5.36
.
7.0 10 bulk solubility limit exceeded 10
the P. luscens biomass at pH 4, 5, 6 and 7 are approximately y60, y75, y85 and
.
y4
y100 mV, respectively. For a total bulk Cu II concentration of 1.0=10 molrl and
.
using the Boltzmann equation the concentrations of Cu II within the diffuse part of the
.
double layer can be roughly calculated. Table 1 shows the amount of Cu II 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 Cu II is exceeded and there should be
.
precipitation of Cu OH within the double layer. Assuming different values for the total
2
.
concentration of Cu II in a system, the pH value at which the double layer concentra-
.
tion of Cu II approximately equals the solubility limit in the bulk solution can be
.
determined for these total concentrations of Cu II . This data is presented in Table 2 for
.
y8 y4
Cu II concentrations from 1=10 to 1=10 molrl.
. . . .
Recent work by Schneider 1995 shows that the sorption of Cu II , Ni II , and Zn II
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 pK of the carboxylate
a
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 Cu II aq. species within the double layer equals the maximum
. .
concentration of Cu II aq. species in the bulk solution as a function of total Cu II in the system
.
Total concentration of Cu II in system The pH at which the concentration of
. .
molrl Cu II aq. within the double layer equals
the maximum concentration in
the bulk of the solution
y4
1=10 5.0
y5
1=10 5.4
y6
1=10 5.8
y7
1=10 6.3
y8
1=10 6.8
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 116
.
other structures Smith, 1989 . From the iep data, assuming that there is no inherent
space charge in the macrophytes, it appears that the pK of the macrophytes is near pH
a
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 Cu II 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 subject-
ing the plant biomass to 50 cycles, analysis of the biomass indicated that there remained
.
a substantial amount of Cu II on the biomass. The data are shown in Table 3. This
.
Cu II was only partially removed with 5% HCl treatment. Thus, there must be both
.
Cu II adsorption onto specific sites and non-specific, reversible, sorption through
.
coulombic interaction between the Cu II 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 precipita-
tion. 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 N
2
determined at 77 K, the vaporization temperature of N , are much less than those
2
Table 3
.
Amount of Cu II remaining in the biomass after 50 loading and elution cycles and after a final elution cycle
with both 0.5% and 5% HCl solutions
Cu concentration natural dead Cu concentration biomass Cu concentration biomass
biomass before sorption after 50 cycles of loading after 50 cycles of loading
and elution cycles and elution using 0.5% and elution using 0.5%
.
mg Curkg biomass HCl solution as eluant HCl solution as eluant
followed by a cycle using
5% HCl as eluant
E. cressipes 46 384 187
P. lucens 19 327 129
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 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 Pretreatment Adsorbate Temperature Surface area Reference
2
. .
K M rg
.
E. crassipes N 77 7.4 Wang 1995
2
.
roots
.
E. crassipes 0.1 M H SO N 77 6. 7 Wang 1995
2 4 2
.
roots
.
E. crassipes N slow drift 77 )150 Schneider et al. 1995
2
.
roots toward
.
equilibrium

E. crassipes N slow drift 77 ;280 This study

2
.
aerial parts toward
.
equilibrium
.
E. crassipes Methylene blue ;298 243 Schneider et al. 1995
.
roots
.
E. crassipes Methylene blue ;298 223 Schneider et al. 1995
.
aerial parts
.
Salinia sp. Methylene blue ;298 274 Schneider 1995
.
Salinia sp. Hydrophobic Methylene blue ;298 278 Ribeiro et al. 1998
surface removed
.
P. lucens Methylene blue ;298 415 Schneider 1995
Soil organic N 77 0.891.1 De Jonge and Mittlemeijer-
2
. .
matter SOM Hazeleger 1996
SOM CO 273 94174 De Jonge and Mittlemeijer-
2
.
Hazeleger 1996
.
SOM Ethylene glycol 298"2 560800 Bower and Gschwend 1952
( )
I.A.H. Schneider et al.rInt. J. Miner. Process. 62 2001 111120 118
. .
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 N . Their suggested alternate mechanisms involve the expansion of
2
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 N at 77 K give values that only represent an Aexternal surfaceB and exclude
2
micropores and inner surfaces. As evidence, their work measuring the surface areas of
SOMs showed that N adsorption at 77 K gave values between 0.89 and 4.94 m
2
rg and
2
that CO adsorption at 273 K gave values between 94 and 174 m
2
rg. Furthermore, the
2
.
work of Rodriguez-Reinoso et al. 1982, 1984 indicates that CO adsorption at 195 and
2
273 K and N adsorption at 90 K yield much greater surface areas of activated carbons
2
than N adsorption at 77 K. However, a slow drift was noted in the latter system. Then,
2
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 adsorption and N
2 2
.
adsorption at 90 K. The conclusion De Jonge and Mittlemeijer-Hazeleger, 1996 is that
N adsorption at 77 K will not measure pores with restrictions less than 0.5 nm unless
2
.
long adsorption times weeks are considered. Since the surface area of SOMs estimated
by microscopic examination is about 0.05 m
2
rg, they also believe that the surface areas

measured by fast N adsorption at 77 K includes pores between 0.5 and 2 nm where

2
. .
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 m
2
rg. However, a slow drift was noted in the
systems and after several days measured areas between 150 and 280 m
2
rg. 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 Hg II sorption onto P. natans biomass
.
electron microscopy evidence shows that, although Hg II was present over the entire
( )
I.A.H. Schneider et al.rInt. 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 Pb II 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 Pb II 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 Strepto-
.
myces sp., although the evidence is not quite as convincing as with Pb II .
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
.
Cu II onto plant biomass surfaces.
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