Environmental Science and Pollution Research

https://doi.org/10.1007/s11356-023-27365-8

RESEARCH ARTICLE

Phosphorus recovery from aqueous solutions using Bioclastic Granules

(Lithothamnium calcareum)
Diego Macedo Veneu1,2 · Gabriel Gonçalves Amaral Silva3 · Alexandre Lioi Nascentes4 · Cristiane Ribeiro Mauad3 ·
Lídia Yokoyama1 · Marisa Bezerra de Mello Monte2 · David Villas Boas de Campos5

Received: 3 January 2023 / Accepted: 27 April 2023

© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023

Abstract
Against the growing world demand for food and the possibility of recovering some nutrients, this work focused on the evalu-
ation of the use of Bioclastic Granules (BG) from the algae Lithothamnium calcareum as sorbent material for the removal/
recovery of phosphorus from aqueous solutions. The main variables that affect the sorption process, pH, initial concentration
of phosphate, and GB, as well as the contact time, were evaluated. The effect of pH was very significant, obtaining the best
results of P­ O43− removal at pH 5. In the coarser granulometric fractions (+ 106 − 150 and + 210 − 300 μm), the best removals
were observed (around 75%). Regarding the initial ­PO43− concentration in the solutions, the highest removal (in the range
of 74 to 78%) was observed in the lowest concentrations (5 to 70 mg ­L−1) and the best uptake (10 to 14 mg ­g−1) at higher
concentrations (200 to 420 mg ­L−1). The ­PO43− sorption data fitted the Freundlich model well, with kF of 1.35 L ­mg−1 and
n of 2.43. A qmax of 14.35 mg ­g−1 was obtained using the Langmuir model. Regarding the sorption data over time, a better
fit to the pseudo-first-order kinetic model was observed, obtaining a calculated qeq of 6.56 mg ­g−1 and a k1 of 0.0073 ­min−1.
The incorporation of P ­ O43− ions in the GB structure was confirmed through the characterization results before and after the
sorption experiments using X-ray fluorescence (FRX) and scanning electron microscopy (SEM) techniques.

Keywords Wastewater treatment · Sorption process · Nutrient recovery · Calcareous algae

Responsible Editor: Guilherme L. Dotto
* Diego Macedo Veneu
diegomveneu@yahoo.com.br
1
Environmental Engineering Program, Federal University
of Rio de Janeiro, Av. Athos da Silveira Ramos, Cidade
Universitária, 149, Bloco A, Rio de Janeiro, RJ 21941‑909,
Brazil
2
Surface Chemistry Laboratory, Centro de Tecnologia
Mineral, Mineral Technology Center, Av. Pedro Calmon,
900, Cidade Universitária, Rio de Janeiro, RJ 21941‑908,
Brazil
3 (Martín-Hernández et al. 2022).
Federal Institute of Education, Science and Technology
of Rio de Janeiro, Campus Rio de Janeiro, Rua Senador
Furtado, 121‑125, Maracanã, Rio de Janeiro, RJ 20260‑100,
Brazil
4
Agricultural and Environmental Engineering Program,
Federal Rural University of Rio de Janeiro, BR 465, Km 07,
Seropédica, RJ 23897‑000, Brazil
5
Brazilian Agricultural Research Corporation, Embrapa Solos,
Rua Jardim Botânico, 1024, Jardim Botânico, Rio de Janeiro,
RJ 22460‑000, Brazil
Introduction
Contamination of water resources by different pollutants
such as PAHs (Onydinma et al. 2021), trace metals (Ukaogo
et al. 2022), NOM (Feng et al. 2022), and nutrients such as
N and P (Salo and Salovius-Laurén 2022) ends up produc-
ing adverse effects on human health, configuring as direct
or indirect precursors of different diseases. An important
impact has been the acceleration of artificial eutrophication
with the increase of nutrient concentration and organic mat-
ter, mainly of phosphate compounds, that tend to enlarge
the biological production in rivers, lakes, and reservoirs
Recently, the water treatment system of Guandu, which
is responsible for most of the potable water destined for the
population of the Metropolitan Region of Rio de Janeiro,
suffered from the introduction of phosphorus and other nutri-
ents in its water. Those contaminants come from effluents
that are discarded without receiving proper treatment, being
from either domestic and/or industrial origin, arising from
river dos Poços and Ipiranga, both rivers that disembogue at

13
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the river Guandu, near the catchment point called Guandu
lake. This guarantees the ideal nutritional portion, so, in
periods of intense solar radiation, algae and cyanobacte-
ria can produce residual substances giving an unpleasant
taste and odor to the water, such as Geosmin (trans-1, 10
dimethyl-trans-9 decalol) and 2-MIB (2-methylisobomeol)
(Kim et al. 1997). In addition, certain species produce, under
specific circumstances, substances that present risk to human
health (Volschan 2022).
The sanitary sewers constitute the main anthropogenic
source of phosphorus in natural waters. According to Larsen
and Gujer (1996), some sanitary effluents, when submitted
to a previous separation, can present a composition with up
to 50% of phosphorus. The compound is inserted through
extremely concentrated detergents along with fecal matter
itself, which is rich in proteins (Piveli 2015). Other industrial
effluents contribute as well to the contamination of waters
with phosphorus, many times due to an intrinsic inefficiency
of the treatment process. Biological systems remove phos-
phorus in low amounts, using it in the production of biomass
through cell growth of heterotrophic bacteria, or even in
mixed cultures involving microalgae and bacteria synergisti-
cally (Ahmed et al. 2022). On the other hand, physicochemi-
cal systems tend to be inefficient when the concentration of
phosphorus is low. In addition, there is a problem on gener-
ating a huge amount of sludge containing metals in general
(Tchobanoglous et al. 2016).
The phosphorus utilized in agricultural practices is nor-
mally obtained from phosphate rock mines that are being
depleted in an alarming rate due to an increase in demand
of this mineral (Lamont et al. 2019). Phosphorous shortages
have very important implications for global food security;
therefore, it should be analyzed in a broader and more inte-
grated sustainability context, providing alternative sources
of phosphorus supply, such as its recovery from effluents
(Neseta and Cordell 2012). According to the Food and Agri-
culture Organization (FAO 2021), growth in the middle-class
population increases the consumption of products, whose
production demands a higher quantity of grains and water,
increasingly pushing agricultural systems. Some treatment
methods to reduce waste in food production and distribution,
thus valuing the waste generated in this chain, are already
well known, such as composting, anaerobic and aerobic
digestion, and the production of biofertilizers (O’Connor
et al. 2021). These methods produce waste that can reduce
the loss of fertile soils and water pollution, as these end up
being deposited in landfills. However, in many cases, these
residues have a more acidic pH and lack other trace elements
necessary for plant nutrition (Reyes-Torres et al. 2018; Fac-
chin et al. 2013). Given the context, the necessity of research
and implementation of innovative techniques becomes clear.
Brazil needs to develop its own technologies for the
obtainment of raw material and new fertilizers geared
13
Environmental Science and Pollution Research
towards the geoclimatic and pedologic conditions of our
soils. In these circumstances, the continental limestone
(known as marine bioclastic limestone) emerges as an
alternative of soil conditioner or nutrients carrier (Veneu
2017). The Bioclastic Granule (BG) is an important min-
eral resource due to its versatility with the possibility of
being utilized as animal feed supplement, human nutrition,
pharmacology/cosmetics, biotechnology (Briand 1976), on
agriculture as a fertilizer and soil corrector (Blunden et al.
1997; Lima et al. 2002; Melo and Furtini Neto 2003), and
most recently, on the treatment of water and effluents (Gray
et al. 2000; Veneu et al. 2017; Caletti 2017; Veneu et al.
2017; Almeida 2018; Veneu et al. 2018a, b; Nogueira 2019;
Melo et al. 2019; Silva et al. 2021).
Wu et al. (2020) highlights the importance of investi-
gating selective phosphate sorption by certain sorbents that
can be reused after the process, adding to the ice a high
concentration of phosphate. It is possible to observe, despite
verified technical work and relevant information about the
material, that technical literature has an insufficient amount
of information and data that could elucidate, in a more con-
sistent way, the application of the enriched Bioclastic Gran-
ule as a soil additive. Through the retention/adsorption of
some elements contained in effluents, especially phosphorus,
the Bioclastic Granule could be posteriorly utilized as a fer-
tilizer/soil conditioner.
The present study evaluated the capacity and efficiency
of Bioclastic Granules (BG) from Lithothamnium calcareum
algae limestone to act as a sorbent material for the treatment
of aqueous solutions containing ­PO43− ions.
Material and methods
Bioclastic Granules and reagents
A sample of approximately 5 kg of Bioclastic Granules
(Lithothamnium calcareum) was provided by the
company Oceana Minerals LTDA with different particle
sizes (+ 210 − 300 μm; + 106 − 150 μm; + 53 − 75 μm,
and − 38 μm). A bar mill followed by separation in series
was utilized for the obtainment of these particles. Initial
tests with synthetic effluents were realized with solutions
prepared with the salt K­ H2PO4 (99%) provided by Sigma-
Aldrich in deionized water.
Sorption batch experiments
Factors affecting BG sorption rate and uptake capacity
were studied on a bench scale. All assays were performed
in 250-mL Erlenmeyer flasks, employing 150 mL of
solution containing ions of P­ O 43−, rotation velocity of
250 rpm in a horizontal platform (CIENLAB CE-720).
Environmental Science and Pollution Research

Succeeding the sorption tests, the BG were deposited adjacent sites. Basically, the Langmuir isotherm equation
through a digital bench centrifuge (CIENTEC CT-6000), has a hyperbolic form, given by Eq. (3):
rotating in 5000 rpm, in falcon tubes of 50 mL. The
qmax KL Ceq
supernatant was filtered with a membrane of cellulose q= (3)
acetate with a pore size of 0.45 μm (Unifil). For 1 + KL Ceq
determination of phosphate ­(PO43−), an ion chromatograph
with conductivity detector model 930 Compact IC Flex where q is the amount of P ­ O43− retained in the solid at equi-
−1
from Metrohm was used. Removal and sorption capacity librium (mg ­g ), qmax is the Langmuir parameter relative to
were calculated through Eqs. (1) and (2), respectively. All sorption capacity (mg g­ −1), kL is the Langmuir constant rela-
assays were performed in triplicate. tive to sorption energy (L ­mg−1), and Ceq is the P ­ O43− con-
−1
centration in solution at equilibrium (mg ­L ).
( )
Ci − Ceq
R= .100 (1) Freundlich isotherm
Ci

The Freundlich isotherm model (Freundlich 1906) assumes

V(Ci − Ceq )
q= (2) that the sorbent material has a heterogeneous surface com-
M posed of several types of sorption sites that saturate dur-
where R is the removal of P ­ O43− ions (%), q is the uptake ing the process, culminating in an exponential decrease in
capacity of ­PO4 ions (mg ­g−1), Ci is the initial ­PO43− con-
3− sorption energy. The Freundlich isotherm model (Eq. (4)) is
centration (mg L ­ O43− concentration at equi-
­ −1), Ceq is the P considered appropriate to describe both multilayer sorption
−1
librium (mg ­L ), V is the volume of the solution containing and can, therefore, be applied to non-ideal systems (Zand
the ­PO43− ions (L), and M is the mass of the BG (g). and Abyaneh 2020).
The following variables were determined: (i) initial 1∕
q = kF Ceq n
(4)
pH, (ii) sorbent concentration, (iii) initial concentration of
phosphate, (iv) particle size, and (v) contact time. Table 1 where q is the amount of P­ O43− retained in the solid at equi-
shows the experimental conditions employed in sorption −1
­ O43− concentration in solution
librium (mg ­g ), Ceq is the P
tests with synthetic effluents. at equilibrium (mg L −1
­ ), kF is a constant that indicates sorp-
tion capacity (L ­mg−1), and n is the constant that indicates
Sorption isotherm sorption strength (L ­mg−1).

Langmuir isotherm
Dubinin‑Radushkevich isotherm
The Langmuir isotherm described initially to predict
Dubinin and Radushkevich (1947) proposed the D-R
the adsorption of gaseous molecules in a solid is widely
isotherm model (Eq. (5)) which represents the adsorp-
used for aqueous systems involving the sorption of ions
tion of vapors and gases on microporous solid surfaces,
in different sorbent materials (Foo and Hameed 2010;
such as activated carbon, through a pore-filling mecha-
Chen et al. 2022). Langmuir (1918) proposed this model
nism. Through the Polanyi potential (Eq. (6)), one can
with the following hypotheses: (i) monolayer adsorption;
get an idea of the adsorption energy distribution. The
(ii) uniform adsorption force on the surface of the
Dubinin-Radushkevich (D-R) model assesses the nature
homogeneous adsorbent; and (iii) no steric hindrance or
of the adsorption and is more general than the Langmuir
lateral interaction between the adsorbed molecules, even at

Table 1  Conditions employed Variable Condition

to determine the influence of
the variables in the process of Solution volume (mL) 150
sorption in batches
Stirring speed (rpm) 250
Initial pH 5; 6; 7; and 8
Particle size (μm) − 38; + 53 − 75; + 106 – 150; and + 210 − 300
BG concentration (g ­L−1) 1; 5; 10; and 20
­ −1)
Phosphate concentration (mg L 5; 15; 30; 50; 70; 100; 150; 200; 300; 350; and 420
Contact time (min) 15; 30; 60; 120; 180; 240; 300; and 360
Temperature (°C) 25

13

isotherm, since it assumes a smooth surface or a constant
adsorption potential.
q = qmax exp(−Bε2 ) (5)
/
(6)
1
𝜀 = RTln(1 + Ceq )
where q is the amount of ­PO43− retained in the solid at
equilibrium (mg ­g −1), q max is the maximum sorption
capacity of the sorbent (mg ­g−1), B is the constant related
to the adsorption energy ­(mol 2 ­k J −2), 𝜀 is the Polanyi
potential (kJ ­m ol −1), R is the universal gas constant
(0.008314 kJ ­mol−1 ­K−1), T is the absolute temperature
(K), and C eq is the ­P O 43− concentration in solution at
equilibrium (mg ­L−1).
The sorption energy value (kJ ­m ol −1) is related to
the constant B, as shown in Eq. (7). It is defined as the
change in free energy when 1 mol of ­PO43− is transferred
from infinity, inside the solution, to the solid surface,
and is related to the sorption phenomenon that happens
in the sorbent/solute system (Wang et al. 2007). If
Es < 8 kJ ­mol−1, the adsorption process is of a physical
nature; if 8 kJ ­mol−1 < Es < 16 kJ ­mol−1, adsorption occurs
by ion exchange; if 16 kJ ­mol−1 < Es, adsorption is of a
chemical nature.
�
Es = 1 √2B (7)
where Es is the mean sorption free energy (kJ ­mol−1).
Temkin isotherm
The Temkin equation model (Eq. (8)) has been proposed
to describe the adsorption of hydrogen on platinum
electrodes within acidic solutions (Febrianto et al.
2009). In this model, the effect of indirect solute/sorbent
interactions on the adsorption isotherms is considered,
assuming that the drop in heat of adsorption is linear due
to the coverage of the layer by the solute/sorbent and non-
logarithmic interactions (Basha et al. 2008).
RT
q= ln(ACeq ) (8)
b
where q is the P ­ O 4 3− amount retained in the solid
at equilibrium (mg ­g −1 ), C eq is the concentration of
­P O 43− in the equilibrium solution (mg L ­ −1), T is the
absolute temperature (K), R is the universal gas constant
(0.008314 kJ ­m ol −1 ­K −1 ), A is the Temkin isotherm
­ g−1), and b is the constant related to the heat
constant (L m
of sorption (kJ ­mol−1).
13
Environmental Science and Pollution Research
Sorption kinetics
Pseudo‑first‑order model
The pseudo-first-order kinetic model was initially introduced
by Lagergren (1907) at the end of the nineteenth century.
According to Ho and McKay (1999), the model can be used
in the form of Eq. (9).
dq
= k1 (qeq − q) (9)
dt
Equation 10 is obtained by integrating Eq. (9) from t = 0
to t = t and qt = 0 to qt = qt:
q = qeq (1 − e−k1 t ) (10)
where qeq is the amount of ­PO43− retained in the solid at
equilibrium (mg ­g−1), q is the amount of ­PO43− retained in
the solid at time “t” (mg g­ −1), and k1 is the pseudo-first-order
reaction velocity constant (g ­mg−1 ­min−1).
Pseudo‑second‑order model
The pseudo-second-order kinetic model was introduced in
the mid-1980s (Blanchar et al. 1984), but it became popular
when Ho and McKay (1999) when evaluating several results
of works by different authors, obtained a better correlation
of the experimental data when used this model. The pseudo-
second-order model is represented by Eq. (11):
dq
= k2 (qeq − q)2 (11)
dt
Equation 12 is obtained by integrating Eq. (11) from t = 0
to t = t and qt = 0 to qt = qt:
qeq 2 k2 t
q= (12)
1 + qeq k2 t
where qeq is the amount of ­PO43− retained in the solid in
equilibrium (mg ­g−1), q is the amount of ­PO43− retained in
the solid at time “t” (mg g­ −1), and k2 is the pseudo-second-
order reaction velocity constant (g ­mg−1 ­min−1).
Characterization
X‑ray fluorescence
Elementary semi-quantitative chemical determination of the
Bioclastic Granule samples before and after the sorption pro-
cess was performed by X-Ray fluorescence spectrometry in
a PanAnalytical equipment, model AXIOS MAX, using the
standardless method for reading the samples. These samples
Environmental Science and Pollution Research

were prepared by melting at a dilution of 1 to 10 using as According to Sondi et al. (2009), the surface of the miner-
flux lithium tetraborate (­Li2B4O7) from Maxxifluxi and als of carbonate in contact with water suffers coordination
0.07 g of lithium iodide (LiI) release agent. reactions with species in solution, such as C ­ a2+, ­CO32−,
3− +
­HCO , and ­CaHCO3 .
Scanning electron microscopy In accordance with a few authors, systems composed
by different types of limestones presented a final pH value
The micrographs of the Bioclastic Granules before and after in the range of 7.5 to 8.0, due to the buffer capacity of
the sorption process were obtained in a scanning electron the carbonate system, once the predominant specie is the
microscope (SEM) FEI Quanta 400, equipped with a Bruker ­HCO3− (Aziz et al. 2008; Sdiri et al. 2012). Figure 2 shows
Xflash 4030 Energy Scattered X-Ray Spectrometry (EDS) the speciation diagram log C as a function of pH, built in
System to evaluate the morphology of the particles. The the computational program computational (MEDUSA—
acquisition and processing of the data generated by the EDS Make Equilibrium Diagrams Using Sophisticated Algo-
were performed using Brucker’s ESPRIT software version rithms, 32 bits).
9.1. The samples were dried in an oven for 24 h at a tem- In fact, as observed in Fig. 2, the increase in pH forms
perature of 60 °C and deposited on carbon adhesive tapes ­ HPO4−, ­CaOH+, ­CaPO42−, ­HPO42−, KOH,
species such as K
2−
supported on metallic disks where they were finally covered ­CO3 , and ­Ca5(PO4)3OH. In this study, in the condition of
with a micrometric gold film from evaporation in a metal- slightly alkali pH (7 to 8.3), it is possible to suggest that
lizing chamber, thus enabling the conduction of electric the concentration of the species C ­ a2+, Ca(OH)2, ­HCO3−,
2− 3− 2−
current. ­CO3 , ­PO4 , and ­HPO4 increases in the surface of the
Bioclastic Granules, working in favor of precipitate forma-
tion as hydroxyapatite ­Ca5(PO4)3OH, and others:
Results and discussion logK=40.46
5Ca2+ + 3PO3− H+ + Ca5 PO4 3 OH(hydroxyapatite)
( )
4 →
Initial pH effect
logK=39.05
Ca2+ + 4H+ + 2PO3−
( )
­ O43− uptake
Ca H2 PO4 2 (monocalcium phosphate)
Figure 1 shows the final concentration and P 4
→

in the pH range of 5 to 8. It is possible to notice with the

increase in the pH value, the final concentrations increased Ca2+
logK=−22.8
→ 2H+ + Ca(OH)2 (calciumhydroxide)
gradually going from 24.1 to 36.7 mg L ­ −1, respectively.
Uptake decreased gradually from pH 5 to 7, with values logK=28.92
of 7.7 mg ­g−1 in pH 5 and 6.4 mg ­g−1 in pH 7. Percent 3Ca2+ + 2PO3−
4
→ Ca3 (PO4 )2 (tricalciumphosphate)
removal decreases from the range of 76–63.8% (pH 5 to
7) to 32% (pH 8); in this value, the highest concentration logK=46.9
4Ca2+ + H+ + 3PO3−
in solution was observed (68.9 mg L ­ −1) and lowest uptake 4
→ Ca4 H(PO4 )3 (tetracalciumphosphate)
−1
(3.2 mg ­g ). The slightly acidic condition of the system
leads to a high dissociation of ­CaCO3 in the surface of the
granules, consequently, better sorption of the ions P ­ O43−.

Fig. 1  Effect of pH in ­PO43− sorption by Bioclastic Granule (initial Fig. 2  Speciation diagram for the C­aCO3 and K ­H2PO4 sys-
concentration of ­PO43−: 100 mg ­L−1; BG concentration: 10 g L.−1; tem ­([CO32−] = 90 mM; ­[Ca2+] = 90 mM; ­[K+] = 1.05 mM; and
particle size: + 106 − 150 μm; temperature: 25 °C; contact time: 6 h) ­[PO4.3−] = 1.05 mM)

13

logK=8.48
Ca2= + CO2− → CaCO3 (calciumcarbonate)
3 tion + 53 − 75 to + 106 − 150 μm, an increase in removal and
Ca2+ + H+ + PO3−
logK=18.95
→ CaHPO4 (calciumhydrogenphosphate)
4
Laurence (1991), studying solubility of different calcium
phosphates in a ternary system (Ca(OH)2, ­H3PO4 e ­H2O),
observed that in slightly acidic regions, every phosphate is
more soluble. In regions of slightly alkali pH, the solubil-
ity of the calcium phosphates decreases in the following
order: hydroxyapatite > tetracalcium phosphate > tricalcium
phosphate > calcium hydrogen phosphate > monocalcium
phosphate. According to Wu et al. (2020), the protonated
phosphate anions interact with the hydrogen bond receptors
with selective ions, such as ­Ca2+, which produces phosphate
complexes. It is observed that other anions, in solution, such
as ­CO32− also had such capacity; however, this anion differs
in the capacity of donating a pair of nonbonding electrons
remaining in the: P­ O43− > ­CO32− order. Therefore, the pre-
dominant mechanism in GB phosphate sorption is spheri-
cal complexation, inner sphere complexation via bonding
variations process, in which the hydrated C ­ O32− groups on
3−
the surface are substituted for ­PO4 anions. As stated by
Wu et al. (2020), the inner sphere complexation involves a
stronger interaction than an external sphere, as observed in
carbonate. However, additional mechanisms, such as elec-
trostatic attraction, and/or precipitate might coexist in the
sorption process.
Particle size effect
In Fig. 3, it is possible to observe the concentration in solu-
tion and uptake of P ­ O43− in the granulometric range of −
38; + 53 − 75; + 106 − 150; and + 210 − 300 μm. The size
increase of the Bioclastic Granule particles has a positive
­ O43− removal. In fraction − 38 μm, the values of
effect in P
removal and uptake were less expressive, corresponding
Fig. 3  Particle size effect in sorption of ­PO43− by Bioclastic Granule
(pH: 5.0; initial concentration of ­PO43−: 80 mg ­L−1; BG concentra-
tion: 10 g L.−1; temperature 25 °C; contact time: 6 h)
13
Environmental Science and Pollution Research
to 49.4% and 4.0 mg ­g−1, respectively. From the frac-
uptake can be noticed, with values of 6.5% and 4.6 mg ­g−1
and 75.6% and 6.1 mg ­g−1, respectively. In the larger size
(+ 210 − 300 μm), the results remain practically the same
to the anterior size (+ 106 − 150 μm). This is a curious
behavior, once that sorbents with less particle sizes usually
presents greater available superficial areas for sorption and
are more susceptible to dissolution in comparison to larger
particles.
Ayoub et al. (2019) evaluated ­PO43− removal by a dolo-
mite (CaMg(CO3)2 from south Beirut, Lebanon) in fixed bed
column systems and observed how the particle size affected
the removal. According to the authors, the best result was
reached in the finest fraction 75 μm (97%), but in the larger
ones + 75 − 105 and + 175 μm, the removal was also high,
corresponding to the values of 90.3% and 93.7%, respec-
tively. Kasprzyk and Gajewska (2019) evaluated a residue of
opoka (enriched carbonate with silicon) pre-processed at a
temperature of 700 °C in the removal of P ­ O43− and observed
−1
a high capacity of uptake (45.6 mg ­g ) applying particles
up to 2.0 mm in size.
What has been observed in the study may be related to
the low variation of surface BET of micropores between dif-
­ 2 ­g−1), suggesting that dis-
ferent fractions (1.44 and 2.81 m
solution reactions of C­ aCO3 do not increase with reduction
in particle size, in other words, exposition of more binding
sites for the formation of new crystals from micropores.
Bioclastic Granule concentration effect
The concentration of the granules is an important factor that
determines the necessary amount of sorbent to remove a
specific amount of P­ O43− in solution. According to Wu et al.
(2020), one of the alternatives for treating effluents contain-
ing phosphorus is chemical precipitation; however, the need
to introduce metal salts into high concentrations brings an
inconvenience that is the high generation of sludge and the
incorporation of these metals into the sludge. In fact, as we
can see in Fig. 4, as BG concentrations increased from 1
to 20 g ­L−1, the removal gradually increased from 13.7%
(1 g ­L−1) to 70.7% (20 g L
­ −1). However, unlike the chemical
precipitation process by metals, the process of phosphorus
sorption generates a highly enriched material with macronu-
trients (Ca, Mg, and P) that can be reused as fertilizers. The
uptake responded in opposition to the concentration, with
the increase in the concentration of Bioclastic Granules, the
values decreased significantly, from 12.5 mg ­g−1 (1 g ­L−1)
to 3.2 mg ­g−1 (20 g ­L−1).
The increase in the removal efficiency with the increase
in the initial concentration of the granules is probably due
to the greater amount of active sorption sites and ­Ca2+,
Ca(OH)2, and ­CaOH+ ions released in solution. Wu et al.
Environmental Science and Pollution Research

the different initial concentrations at pH 5.0; BG concentra-

tion of 10 g L­ −1; particle size: + 106 − 150 μm; temperature:
25 °C; contact time: 6 h.
As shown in Table 2, the ­PO43− ions present a similar
behavior, with the increase in the initial concentration from
5 to 70 mg ­L−1, the removal values remain practically the
same, in the range of 74 to 78%. In the concentration of
100 mg ­L−1, removal decreases gradually from 66 to 34%
in the initial concentration of 420 mg L ­ −1. Kasprzyka
et al. (2018) noticed a similar pattern in this study, appli-
cating a bentonite modified with lanthanum (Phoslock®)
for the removal of phosphorus in concentrated solutions,
Fig. 4  Effect of the initial concentration of BG on the sorption of varying from 5 to 100 mg L ­ −1. According to the authors,
­PO43− (pH: 5.0; initial concentration of P­ O43−: 92 mg L.−1; particle removal was practically the same (> 95%) in all different
size: + 106 − 150 μm; temperature: 25 °C; contact time: 6 h) concentrations.
The uptake values, with the increase in P ­ O43− concen-
tration in solution, also increase gradually, going from 0.38
(2020) describes that the presence of calcium and mag- (5 mg ­L−1) to 14.3 mg ­g−1 (420 mg ­L−1). The fact that an
nesium generally increases the phosphate removal capac- increase of ions P ­ O43− in solution does not significantly
ity through surface precipitation (co-precipitation of Ca-P increase the removal rates may be associated with the epitax-
and Mg-P). Some studies describe that the solubility of ial growth of a fine layer of calcium phosphate crystals in the
hydroxyapatite begins to decrease from pH 4.1, initiating the surface of the granules, during the process of sorption. This
formation of this species in solution (Aljerf and Choukaife layer may prevent the C ­ aCO3 dissolution, forming a stagna-
2017; Choukaife and Aljerf 2017). Some species of soluble tion layer, impeding the creation process of new precipitation
hydroxides in the pH range under study may promote the nucleus and, posteriorly, new crystals. A few authors describe
formation of more stable solid species, since they serve as that the proportion of calcite and aragonite that composes the
precipitation nuclei at the solid-solution interface. In real material may also interfere. The aragonite, for instance, has
processes, higher concentrations of Bioclastic Granules sorption capabilities much higher than calcite (Prieto et al.
(BG) are applied to ensure complete removal of ­PO43− in 2003; Cubillas et al. 2005; Köhler et al. 2007).
effluents, once the limits stablished by responsible organs In accordance with Veneu (2017), it is always necessary
be satisfied. Caletti (2017) applicating BG for the treatment to identify the maximum potential of saturation of a sorb-
of raw leachate observed that an increase in the initial con- ent, so the tests may be realized in the highest initial solute
centration of the granules was necessary to reach expressive concentration as possible. This value of maximum uptake of
values in removal. According to the author, with 40 g L ­ −1 saturation can be calculated through adsorption isotherms.
of the granules, it was possible to remove around 81.5% of
phosphorus of the effluent.
These results suggest that the sorbent’s concentration
must be taken into consideration when utilizing materials Table 2  Effect of initial concentration of ­PO43− in the removal and
based on ­CaCO3 with the final objective of controlling cost/ uptake by Bioclastic Granules
benefit. Both uptake capacity and efficiency of removal of Initial concentration ­PO43− Removal (%) q (mg g­ −1)
­PO43− ions are equally important in the process of sorption. (mg ­L−1)
The concentration of 10 g ­L−1 of Bioclastic Granules was
5 76.47 0.38
maintained in the following tests.
15 78.58 1.18
30 78.06 2.34
Initial concentration of ­PO43− effect
50 74.39 3.74
70 74.18 5.17
The rate that the ions are removed from the liquid phase to
100 66.35 6.64
solid phase is generally described in comparison with their
150 51.28 7.69
initial concentration, making it a very important variable of
200 52.35 10.47
the process. Sorption tests were realized utilizing Bioclastic
300 35.97 10.79
Granules and different solutions with initial concentrations
350 33.80 11.83
of ­PO43− in the range of 5 to 420 mg ­L−1. Table 2 shows
420 34.05 14.30
the values for the removal and uptake of ­PO43− ions with

13

Fig. 5  The ­PO43− ions sorption isotherm (pH: 5.0; initial concentra-
tion of the BG: 10 g L.−1; particle size: + 106 − 150 μm; temperature:
25 °C; contact time: 6 h)
Sorption isotherms
The adsorption isotherms were built with data of the equi-
librium, aiming the determination of important parameters,
for instance, the theoretical saturation capacity of the Bio-
clastic Granules for the P ­ O43− ions and the type of mech-
anism in the sorption process. The tests were realized in
the initial concentrations of 5 to 420 mg ­L−1 with the final
objective of obtaining the maximum saturation capacity of
the BG. Figure 5 shows the experimental data of the quan-
­ O43− ion in sorption (q in mg g­ −1) as a function of
tity of P
the concentration (mg L ­ −1) of these ions in solution. The
dashed lines show the isotherms profiles generated through
the model of Langmuir, Freundlich, Dubinin-Radushk-
evich (D-R), and Temkin. Table 3 contains the parameters
obtained from the models of isotherms, and the respective
correlation coefficients.
In Fig. 5, the profile of P ­ O 43− uptake data can be
observed, being similar to the “L” type, in other words,
Langmuir’s type. This isotherm is used for solids with rela-
tively small external surfaces and when the relation between
solute concentration in solution and in sorption decreases
with the increase of solute (Aljerf 2018). They present with
a concave curve, suggesting a progressive saturation of the
solid, what, in this case, may be related to a stagnation.
Based on the values obtained and shown in Table 3, the
­PO43− sorption data were better suited to the Langmuir
Table 3  Parameters obtained
Langmuir
from the isotherm models and
their correlation coefficients qmax (mg ­g−1)
14.35
Dubinin-Radushkevich
qmax (mg ­g−1)
10.97
13
Environmental Science and Pollution Research
(R2 = 0.965) and Freundlich (R2 = 0.961) models. Accord-
ing to the images obtained with the SEM, it was possible
to observe that the surface of the BG after sorption does
not present a well-defined monolayer as recommended by
the Langmuir model, which can be justified initially by
the sorption of P ­ O43− at the interface, thus forming this
monolayer, and as the crystals are formed, a second stage
begins, that of crystal growth, the formation of more het-
erogeneous solids, as recommended by the Freundlich
model, culminating in very close correlation coefficients
comparing the two models.
In face of this statement, the q max values obtained
through the Langmuir model (qmax = 14.35 mg ­g−1) and
Dubinin-Radushkevich (10.97 mg ­g−1) may be treated cau-
tiously. The values of qmax represent the maximum of sorp-
tion capacity when the surface of the sorbent is completely
covered (Aljerf 2018). High kL values would indicate a
high affinity between the P ­ O43− ions and the Bioclastic
Granules, reflecting in a steep isotherm curve. However,
it was not observed, with a low value of k L (0.0248 L
­mg−1) as expected, once that sorption through precipita-
tion mechanism and crystal growth is not as fast as the
adsorption mechanism.
According to Wang et al. (2007), the average free energy
in sorption Es is related to the type of sorption. For values of
Es < 8 kJ ­mol−1, which is the case in this study, that presents
the value of Es = 0.1 kJ ­mol−1, what might be good, once
the enriched granules will be utilized posteriorly as a soil
fertilizer.
In the Freundlich model, kF represents a measurement
relative to the adsorption capacity, and n is related to the
adsorption intensity; in other words, values > 1 indicate that
the ions are not going through a favorable sorption process.
In Table 3, it is possible to observe that the value of n (2.43
L ­mg−1) demonstrates a good distribution of ­PO43− ions in
the BG. According to Frimmel and Huber (1996), a rela-
tively light inclination n >  > 1 indicates that the intensity of
sorption is high in every concentration range of the study,
while a steeper inclination (n < 1) means that the intensity
of sorption is only high in high concentrations, decreasing
at lower ones. In fact, as previously discussed, in the con-
centrations of 5 to 70 mg ­L−1 of ­PO43−, the most significant
removals were obtained, although they had lesser uptake,
characterizing an n >  > 1 and a light inclination isotherm.
Freundlich
kL (L ­mg−1) R2 kF (L ­mg−1) n R2
0.0248 0.965 1.35 2.43 0.961
Temkin
β ­(mg2 ­kJ−2) R2 ­ g−1)
A (L m b (kJ ­mol−1) R2
42.67 0.871 0.52 1.00 0.949
Environmental Science and Pollution Research
As observed in Table 3, the sorption data of ­PO43− by the
Bioclastic Granules adjust well to Temkin model, with val-
ues of the constants A and b of 0.52 L ­mg−1 and 1.0 kJ ­mol−1,
respectively. In this study, this high correlation coefficient
for the Temkin isotherm may have occurred due to a linear
dependency of heat of sorption in relation to the nucleation
process and the growth of heterogenous crystals in a layer
formed in the surface of the Bioclastic Granules.
Kasprzyk et al. (2021) evaluated three distinct materials
for the phosphorus removal, in bentonite modified with lan-
thanum (Phoslock®), a byproduct of powder carbonate rock,
with a high content of silicon (Rockfos®) and a residue of
water treatment (DWTR) with different contents of Fe and
Mn. According to the authors, the three materials showed
sorption data that adjust well to the Freundlich model, with
correlation coefficients of 0.92, 0.99, and 1.00, respectively.
The values of qmax obtained through the isotherm model of
Langmuir were 158.7 mg ­g−1 for Phoslock®, 256.4 mg ­g−1
for Rockfos®, and 6.9 mg ­g−1 for DWTR.
Kong et al. (2018) obtained a sorbent material for phos-
phorus ions from a calcined sludge at 800 °C with different
proportions for ­CaCO3:sludge (0:1, 1:2, and 1:1). According
to the authors, the sorption data for the three proportions
adjust well to Langmuir model, presenting a R2 = 0,999,
while the calculated coefficients through the Freundlich
model were < 0.70. The values of q max for the relation
0:1, 1:2, and 1:1 were 22.04, 116.82, and 97.56 mg ­g−1,
respectively.
Sorption kinetics
One of the main information that we may obtain from the
kinetic studies of sorption is the sorption rate. It determines
the necessary contact time with the surface of the sorption
and solution, and with that information, it is possible to scale
the size of the reactor. According to Davis et al. (1987),
sorption rates of ions prevenient of minerals based on cal-
cium carbonate are generally characterized by process that
depend on the physicochemical nature of the material and
ions in the process of sorption, with a half-life varying from
a few minutes to even days.
The experimental uptake data (q) were applied in the
kinetic models of pseudo-first and pseudo-second order
for the verification of the order and sorption velocity of the
­PO43− ions and the BG. Figure 6 shows the experimental
data of uptake through time, with the corresponding lines
of the models of pseudo-first and pseudo-second order for
the sorption of ­PO43− ions.
Figure 6 shows a gradual growth in the uptake values,
with an initial value of 0.54 mg ­g−1 in the first 15 min, rising
to 53.2 mg ­g−1 in the mark of 180 min. From that point on,
the uptake varies in the range of 53 to 57 mg ­g−1 until the
mark of 360 min, suggesting a reduction on the sorption rate
Fig. 6  Reactions of pseudo-first and pseudo-second order for the
sorption of P ­ O43− ions with the Bioclastic Granules (pH: 5.0; BG
concentration: 10 g ­L−1; initial concentration of ­PO43−: 100 mg L.−1;
particle size + 106 − 150 μm; temperature: 25 °C)
in that period of the reaction. In fact, the sorption rates of
­PO43− ions in the Bioclastic Granules are related with inter-
action with species as C ­ a2+, ­CaOH+, Ca(OH)2, ­HCO3−, and
2−
­HPO4 , that depend on the pH of the solution. The early
stages of the sorption process are quicker due to reactions in
the surface of the sorbent, while slower process in the final
stages occur due to a structural diffusion and recrystalliza-
tion in the surface of the BG.
This behavior observed in the sorption process in respect
to the recrystallization rate of ionic solids is consistent with
the surface model proposed by Lahann and Siebert (1982)
that includes a hydrated calcium carbonate layer in the disor-
dered surface of the calcite that crystallizes over the calcite.
The existence of this stage is supported by experimental
observations that shows that dissolution and precipitation
of calcite rates are generally controlled by a surface reac-
tion instead of a diffusion of the reactants (Nancollasg and
Reddy 1971).
Table 4 shows the kinetic parameters obtained with the
utilization of pseudo-first- and pseudo-second-order mod-
els for the P­ O43−. It is possible to verify that the kinetic
data obtained adjusted well to the kinetic models, with
R2 > 0.97. However, the kinetic model of pseudo-first-order
presents a R2 value of 0.979 and, consequently, a calculated
qe value (6.56 mg ­g−1) closer to the one obtained experi-
mentally (5.88 mg ­g−1), and a k1 value of 0.0073 ­min−1.
Kasprzyk et al. (2021) evaluating a calcium carbonate based
by product for the removal of phosphorus related that the
pseudo-first-order model presented a good correlation coef-
ficient and qe and k1 values of 7.9 mg ­g−1 and 0.0013 ­min−1,
respectively.
Chen et al. (2014) evaluating the application of a ceramic
biomaterial calcite/montmorillonite/starch based (1:1:1)
for the removal of P ­ O43− observed that in the early stages
of sorption, the ions entered the sorption process in the
external surface of the sorbent with a high rate of sorption.
13
 Environmental Science and Pollution Research

­ O43− ions with the

Table 4  Kinetic parameters obtained from the kinetic models of pseudo-first- and pseudo-second- order for the sorption of P
Bioclastic Granules
Pseudo-first-order Pseudo-second-order qeq exp (mg g­ −1)
qeq (mg ­g−1) k1 ­(min−1) R2 qeq (mg ­g−1) k2 (g ­mg−1 ­min−1) R2

6.5652 0.0073 0.979 9.2130 0.0006 0.973 5.88

Posteriorly, the sorption in the external surface reached a
saturation stage. According to the authors, when the sorption
data was applied to a pseudo-first model, a R2 of 0.979, qe of
9.5 mg ­g−1, and a k1 of 0.017 ­min−1 were obtained.
Characterization
X‑ray fluorescence
According to Gubernat et al. (2020) phosphorus adsor-
bent materials must have elements such as Ca, Mg, Fe,
and Al that end up functioning as phosphorus binders. The
mechanism of phosphate sorption by Fe and Al can occur
through the exchange of ligands, and for Ca and Mg, the
removal of phosphates is carried out through the precipita-
tion of poorly soluble calcium phosphates or struvite (Wu
et al. 2006).

Table 5 shows obtained values of the oxides of the constitu-
ents of the Bioclastic Granules through X-ray fluorescence
(XRF). The calcium oxide represents 45.7% of the material,
in smaller proportions, magnesium oxide (MgO—5.6%), and
silicon oxide ­(SiO2—2.7%). The remaining oxides repre-
sent slightly less than 2.2% of the material. Approximately
43.8% of the material was eliminated in the process by fire
loss. Vila (2012) obtained similar percentages of fire loss
(43.5–45.3%) for different aragonite-based biomaterials,
attributing this percentage to organic matter and water.
Several authors obtained similar compositions to the ones
found in this research for carbonated minerals. Silva et al.
(2010) characterize two biomaterials (oyster shells and mus-
sels); it contained majorly CaO, corresponding to 56.1% of
oyster shells and 53.8% of mussels. The remaining oxides
represent less than 1% of their composition. Zeng et al.
(2003) evaluating the removal of P in two volcanic soils
observed that it was possible to incorporate about 0.566 to
0.909 mgP ­g−1 of volcanic soils that had high levels of ­SiO2
(42.4 to 47.2%), ­Al2O3 (11.2 to 12.9%), and ­Fe2O3 (9.53 to
7.74%) and low contents of CaO (2.21 to 1.58) and MgO
(0.908 to 0.791). According to Table 4, it was possible to
remove about 8.29 mgP g­ −1 of GB (equivalent to 1.9% ­P2O5)
and a reduction in the contents referring to loss on fire, CaO
and MgO, evidencing a redistribution of elements in the
chemical structure of BG as a function of the sorption of
­PO43− on the surface of the material.
Scanning electron microscopy
With the objective of evaluating the morphology of the
Bioclastic Granule particles before and after the process of
­ O43−, scanning electron microscopy analysis
sorption with P
was made. In Fig. 7A, C, a particle of the granule can be
observed before and after the sorption process, respectively.
In Fig. 7A, the particle presents an irregular surface, with
the predominance of cavities of different sizes and small
fragments inside and in its radius. After sorption, the parti-
cle presents different clear crystalline solids, that disorderly
grows from its nucleus, giving birth to a new crystalline
phase in the surface of the Bioclastic Granules.
As reported by Davis et al. (1987), among the main
mechanisms of reaction of an aqueous solute with the
surface of a pre-existing solid phase, the adsorption and
precipitation are considerably similar; they still differ
in their geometry. The adsorption is generally bidimen-
sional, while precipitation in a surface is tridimensional.
Sposito (1984) describes the term precipitation as being a
process that implicates on the growth of a new solid phase
that propagates in a molecular unity repeatedly in three
dimensions. Farley et al. (1985) utilized the term surface
precipitation to describe a multilayer adsorption process,
what may include the formation of an ordinated solid
solution as the growing phase of a crystal. In this study,
the ­PO43− apparently forms precipitates in the surface of

Table 5  Values of the Bioclastic

Component (%)—before of the sorption
Granule oxides obtained by
XRF CaO Fire loss MgO SiO2 Na2O Al2O3 Cl SO3 Fe2O3 SrO P2O5 K2O MnO
45.7 43.8 5.6 2.7 0.49 0.24 0.27 0.54 0.21 0.24 < 0.1 0.11 < 0.1

Component (%)—after of the sorption

CaO Fire loss MgO SiO2 Na2O Al2O3 Cl SO3 Fe2O3 SrO P2O5 K2O MnO
44.8 39.1 3.2 8.8 0.48 0.45 < 0.1 0.44 0.34 0.37 1.9 0.11 < 0.2

13
Environmental Science and Pollution Research
A B
C D
Fig. 7  Images obtained by SEM and EDS spectrums of Bioclastic Granules before and after sorption with ions ­PO43−: A BG with increase
of × 2000; B spectrum before sorption; C BG + ­PO43− with an increase of × 500; and D spectrum after sorption
the Bioclastic Granules, originating a multilayer sorption
process that forms a new ordinated solid solution fol-
lowed by the growth of a new crystal as stated in Fig. 7C.
In Fig. 7B, D, spectrums obtained in the surface of a Bio-
clastic Granule particle by dispersive energy X-ray can be
­ O43− ions, respec-
observed, before and after sorption with P
tively. In Fig. 7D, before the sorption process, the spectrum
presents three sharp peaks referring to the elements, Ca, O,
and C, characteristic of the mineral C ­ aCO3, besides peaks
of the elements Mg and Au that were utilized in the metal-
lization process. After sorption with ions P­ O43− (Fig. 7D),
the three expressive peaks of Ca, O, and C practically main-
tained unaltered, but a new one of P appeared, evidenc-
ing a kind of exchange mechanism between H ­ CO3− and
2−
­HPO4 ions that appear in the spectrum in the form of P and
reduction of C and O elements after the sorption process.
Conclusions
Based on the results, it can be concluded that at pH 5,
GB presented the most expressive values of removal
(76%). In general, when the initial concentrations of
­P O 43− were increased from 5 to 420 mg ­L −1, the high-
est removal (76.4%) was observed at the concentration of
5 mg ­L−1 and the highest uptake (14.3 mg ­g−1) at a con-
centration of 420 mg ­L−1. The sorption data fitted well
to the Langmuir isotherm models (R 2 = 0.965) showing
q max values of 14.35 mg ­g −1 and k L of 0.0248 L m ­ g −1
2
and Freundlich (R = 0.961) showing kF values of 1.35 L
­mg−1 and n of 2.43. The uptake data best fitted the pseudo-
first-order kinetic model (R2 = 0.979) and calculated qeq
of 6.56 mg ­g−1 and k1 of 0.0073 ­min−1. Regarding char-
acterization, the Bioclastic Granules have a chemical
13

composition predominantly in the form of CaO (45.7%),
followed by MgO (5.6%) and S ­ iO2 (2.7%). After the sorp-
tion process, it was possible to verify a ­P2O5 content cor-
responding to 1.9%. The SEM associated with the EDS
showed that the GB has a very irregular surface, with a
predominance of cavities of different sizes that are later
filled by small precipitation nuclei that evolve into small
crystals on the surface of the GB presenting element P in
its composition.
Author contribution Conceptualization: Diego Macedo Veneu, Gabriel
Gonçalves Amaral Silva, and Cristiane Ribeiro Mauad; methodology:
Diego Macedo Veneu, Gabriel Gonçalves Amaral Silva, and Alexan-
dre Lioi Nascentes; investigation: Diego Macedo Veneu, Gabriel Gon-
çalves Amaral Silva, Cristiane Ribeiro Mauad, and David Villas Boas
de Campos; writing—original draft preparation: Diego Macedo Veneu,
Gabriel Gonçalves Amaral Silva, Lidia Yokoyama, Marisa Bezerra de
Mello Monte, Alexandre Lioi Nascentes, and David Villas Boas de
Campos; project administration: Lidia Yokoyama, Marisa Bezerra de
Mello Monte, and David Villas Boas de Campos. All authors have read
and agreed to the published version of the manuscript.
Funding This study was funded by the Brazilian National Council for
Scientific and Technological Development (CNPq) and Carlos Chagas
Filho Foundation for Research Support of the State of Rio de Janeiro
(Faperj).
Data availability All data generated or analyzed during this study are
included in this published article.
Declarations
Ethics approval and consent to participate Not applicable.
Consent for publication Not applicable.
Competing interests The authors declare no competing interests.
References
Ahmed SF, Mofijur M, Parisa TA, Islam N, Kusumo F, Inayat A, Le
VG, Badruddin IA, Khan TMY, Ong HC (2022) Progress and
challenges of contaminate removal from wastewater using micro-
algae biomass. Chemosphere 286:131656. https://​doi.​org/​10.​
1016/j.​chemo​sphere.​2021.​131656
Aljerf L (2018) High-efficiency extraction of bromocresol purple dye
and heavy metals as chromium from industrial effluent by adsorp-
tion onto a modified surface of zeolite: kinetics and equilibrium
study. J Environ Manage 225:120–132. https://​doi.​org/​10.​1016/j.​
jenvm​an.​2018.​07.​048
Aljerf L, Choukaife AE (2017) Hydroxyapatite and fluoroapatite
behavior with pH change. Int Medical J 24:407–410
Almeida AES (2018) Removal of iron in water by adsorption in batch
and fixed bed using Lithothamnium calcareum seaweed in differ-
ent treatments. [D.Sc. thesi] Minas Gerais: Federal University of
Lavras. [In Portuguese]
Ayoub GM, Kalinian H, Zayyat R (2019) Efficient phosphate removal
from contaminated water using functional raw dolomite powder.
SN Appl Sci 1:802. https://​doi.​org/​10.​1007/​s42452-​019-​0833-5
13
Environmental Science and Pollution Research
Aziz HA, Adlan MN, Ariffin KS (2008) Heavy metals (Cd, Pb, Zn, Ni,
Cu and Cr(III)) removal from water in Malaysia: post treatment by
high quality limestone. Bioresour Technol 99:1578–1583. https://​
doi.​org/​10.​1016/j.​biort​ech.​2007.​04.​007
Basha S, Murthy ZVP, Jha B (2008) Sorption of Hg(II) from aqueous
solutions onto Carica papaya: application of isotherms. Ind Eng
Chem Res 47:980–986. https://​doi.​org/​10.​1021/​ie071​210o
Blanchar G, Maunaye M, Martin G (1984) Removal of heavy metals
from waters by means of natural zeolites. Water Res 18:1501–
1507. https://​doi.​org/​10.​1016/​0043-​1354(84)​90124-6
Blunden G, Campbel SA, Smith JR, Guiry MD, Hession CC, Griffin
RL (1997) Chemical and physical characterization on calcified red
algal deposits known as mäerl. J Appl Phycol 9:11–17. https://d​ oi.​
org/​10.​1023/A:​10079​65325​442
Briand X (1976) Lithothamne – tradition from the past, to the future in
the Agrochemistry. S.E.M.A., B.P. 65, Pointrieux.
Caletti RPK (2017) Efficiency of Lithothamnium calcareum in removal of
phosphorus from landfill leachate. [M.Sc. dissertation] Rio de Janeiro:
Federal Rural University of Rio de Janeiro; 2017. [In Portuguese]
Chen X, Hossain MF, Duan C, Lu J, Tsang YF, Islam MS, Zhou Y
(2022) Isotherm models for adsorption of heavy metals from water
- a review. Chemosphere 307:135545. https://​doi.​org/​10.​1016/j.​
chemo​sphere.​2022.​135545
Chen N, Hu W, Feng C, Zhang Z (2014) Removal of phosphorus
from water using scallop shell synthesized ceramic biomateri-
als. Environ Earth Sci 2133–2142. https://​d oi.​o rg/​1 0.​1 007/​
s12665-​013-​2618-2
Choukaife AE, Aljerf L (2017) A descriptive study - in vitro: new
validated method for checking Hap and Fap behaviours. Int Medi-
cal J 24:394–397
Cubillas P, Köhle S, Prieto M, Causserand C, Oelkers EH (2005) How
do mineral coatings affect dissolution rates? An experimental
study of coupled ­CaCO3 dissolution-CdCO3 precipitation. Geo-
chim Cosmochim Acta 69:5459–5476. https://​doi.​org/​10.​1016/j.​
gca.​2005.​07.​016
Davis JA, Fuller CC, Cook AD (1987) A model for trace metal sorp-
tion processes at the calcite surface: adsorption of C ­ d2+ and
subsequent solid solution formation. Geochim Cosmochim Acta
51:1477–1490. https://​doi.​org/​10.​1016/​0016-​7037(87)​90330-9
Dubinin M, Radushkevich L (1947) The equation of the characteristic
curve of activated charcoal. Proceedings of the Academy of Sci-
ences of the USSR. Phys Chem Sect 55:331–337
Facchin V, Cavinato C, Fatone F, Pavan P, Cecchi F, Bolzonella D
(2013) Effect of trace element supplementation on the mesophilic
anaerobic digestion of foodwaste in batch trials: the influence of
inoculum origin. Biochem Eng J 70:71–77. https://​doi.​org/​10.​
1016/j.​bej.​2012.​10.​004
FAO - Food and Agriculture Organization of the United Nations (2021)
The State of Food Security and Nutrition In The World 2021.
FAO, IFAD, UNICEF, WFP and WHO [Internet] 2021; [cited
2021 jun 25]. Available from: https://​www.​fao.​org/​docum​ents/​
card/​en/c/​cb447​4en
Farley KJ, Dzombak DA, Morel FMM (1985) A surface precipitation
model for the sorption of cations on metal oxides. J Colloid Interface
Sci 106:226–242. https://​doi.​org/​10.​1016/​0021-​9797(85)​90400-X
Febrianto J, Kosasih AN, Sunarso J, Ju Y, Indraswati N, Ismadji S (2009)
Equilibrium and kinetic studies in adsorption of heavy metals using
biosorbent: a summary of recent studies. J Hazard Mater 162:616–
645. https://​doi.​org/​10.​1016/j.​jhazm​at.​2008.​06.​042
Feng H, Liang YN, Hu X (2022) Natural organic matter (NOM), an
underexplored resource for environmental conservation and reme-
diation. Mater Today Sustain 19:100159. https://d​ oi.o​ rg/1​ 0.1​ 016/j.​
mtsust.​2022.​100159
Foo KY, Hameed BH (2010) Insights into the modeling of adsorp-
tion isotherm systems. Chem Eng J 156:2–10. https://​doi.​org/​10.​
1016/j.​cej.​2009.​09.​013
Environmental Science and Pollution Research
Freundlich HMF (1906) Über die adsorption in lösungen. Z Phys Chem
57:385–470. https://​doi.​org/​10.​1515/​zpch-​1907-​5723
Frimmel FH, Huber L (1996) Influence of humic substances on the
aquatic sorption of heavy metals on defined minerals phases.
Environ Int 22:507–517. https://​doi.​org/​10.​1016/​0160-​4120(96)​
00040-2
Gray S, Kinross J, Read P, Marland A (2000) The nutrient assimilative
capacity of maerl as a substrate in constructed wetland systems
for waste treatment. Water Resour 34(8):2183–2190. https://​doi.​
org/​10.​1016/​S0043-​1354(99)​00414-5
Gubernat S, Maslon A, Czarnota J, Koszelnik P (2020) Reactive mate-
rials in the removal of phosphorus compounds from wastewater—
a review. Materials 131–26. https://​doi.​org/​10.​3390/​ma131​53377
Ho Y, McKay G (1999) Pseudo-second order model for sorption pro-
cesses. Process Biochem 34:451–465. https://​doi.​org/​10.​1016/​
S0032-​9592(98)​00112-5
Kasprzyk M, Gajewska M (2019) Phosphorus removal by application of
natural and semi-natural materials for possible recovery according to
assumptions of circular economy and closed circuit of P. Sci Total
Environ 650:249–256. https://​doi.​org/​10.​1016/j.​scito​tenv.​2018.​09.​034
Kasprzyk M, Czerwionka K, Gajewska M (2021) Waste materials
assessment for phosphorus adsorption toward sustainable appli-
cation in circular economy. Resour Conserv Recy 168:105335.
https://​doi.​org/​10.​1016/j.​resco​nrec.​2020.​105335
Kasprzyka M, Obarska-Pempkowiaka H, Masib F, Gajewska M (2018)
Possibilities of Phoslock® application to remove phosphorus
compounds from wastewater treated in hybrid wetlands. Ecol Eng
122:84–90. https://​doi.​org/​10.​1016/j.​ecole​ng.​2018.​07.​020
Kim Y, Lee Y, Gee CS, Choi E (1997) Treatment of taste and odor
causing substances in drinking water. Water Sci Technol 35:29–
36. https://​doi.​org/​10.​1016/​S0273-​1223(97)​00148-0
Köhler SJ, Cubillas P, Blanco JDR, Bauer C, Prieto M (2007) Removal
of cadmium from wastewaters by aragonite shells and the influ-
ence of other divalent cations. Environ Sci Technol 41:112–118.
https://​doi.​org/​10.​1021/​es060​756j
Kong L, Han M, Shih K, Su M, Diao Z, Long J, Chen D, Hou L,
Peng Y (2018) Nano-rod Ca-decorated sludge derived carbon for
removal of phosphorus. Environ Pollut 233:698–705. https://​doi.​
org/​10.​1016/j.​envpol.​2017.​10.​099
Lagergren SY (1907) Zur Theorie der sogenannten adsorption gelöster
Stoffe. Kungliga Svenska Vetenskapsakad. Handlingar 24:1–39.
https://​doi.​org/​10.​1007/​BF015​01332
Lahann RW, Siebert RM (1982) A kinetic model for distribution coef-
ficients and application to Mg-calcites. Geochim Cosmochim Acta
46:2229–2237. https://​doi.​org/​10.​1016/​0016-​7037(82)​90197-1
Lamont K, Pensini E, Daguppati P, Rudra R, van de Vegte J, Lev-
angie J (2019) Natural reusable calcium-rich adsorbent for the
removal of phosphorus from water: proof of concept of a circular
economy. Can J Civ Eng 46:458–461. https://​doi.​org/​10.​1139/​
cjce-​2018-​0512
Langmuir I (1918) The adsorption of gases on plane surfaces of glass,
mica, and platinum. J Am Chem Soc 40:1361–1403. https://​doi.​
org/​10.​1021/​ja022​42a004
Larsen TA, Gujer W (1996) Separate management of anthropogenic
nutrient solutions (human urine). Water Sci Technol 34:87–94.
https://​doi.​org/​10.​1016/​0273-​1223(96)​00560-4
Laurence CC (1991) Development of self-setting calcium phosphate
cements. J Ceram Soc Jpn 99(10):954–964. https://​doi.​org/​10.​
2109/​jcersj.​99.​954
Lima LML, Fernandes DL, Souza MWR, Melo PC, Teodoro REF,
Luz JMQ, Almeida FG, Carvalho JOM (2002) Lithothamnium
calcareum doses on the development of sweet pepper plants. Hort
Bras 20:2 (In Portuguese)
Martín-Hernández E, Hu Y, Zavala VM, Martín M, Ruiz-Mercado GJ
(2022) Analysis of incentive policies for phosphorus recovery at
livestock facilities in the Great Lakes area. Resour Conserv Recycl
177:105973. https://​doi.​org/​10.​1016/j.​resco​nrec.​2021.​105973
Melo AFSR, Ribeiro ICA, Fia FR, Fia R, Matos MP (2019) Phosphorus
recovery from wastewater via Lithothamnium calcareum. In: 30th
Brazilian Congress of Sanitary and Environmental Engineering;
2019 Jun 16–19; Rio Grande do Norte, Brazil, 9p. [In Portuguese]
Melo PC, FurtiniNeto AE (2003) Evaluation of Lithothamnium as a soil
acidity corrector and source of nutrients for common bean. Ciênc
Agrotec 27(3):508–519. https://​doi.​org/​10.​1590/​S1413-​70542​
00300​03000​03. (In Portuguese)
Nancollasg H, Reddy MM (1971) The crystalltzation of calcium car-
bonate II. Calcite growth mechanism. J Colloid Interface Sci
37:824–830. https://​doi.​org/​10.​1016/​0021-​9797(71)​90363-8
Neseta TSS, Cordell D (2012) Global phosphorus scarcity: identify-
ing synergies for a sustainable future. J Sci Food Agric 92:2–6.
https://​doi.​org/​10.​1002/​jsfa.​4650
Nogueira MFM (2019) Study of the effect of the addition of bioclas-
tic granular material (Lithothamnium calcareum) applied in the
removal of organic load and pollutants in the treatment of effluents
in an aerobic bioreactor. [M.Sc. dissertation] Rio de Janeiro: Fed-
eral Rural University of Rio de Janeiro. [In Portuguese]
O’Connor J, Hoang SA, Bradney L, Dutta S, Xiong X, Tsang DCW,
Ramadass K, Vinu A, Kirkham MB, Bolan NS (2021) A review
on the valorisation of food waste as a nutrient source and soil
amendment. Environ Pollut 272:115985. https://d​ oi.o​ rg/1​ 0.1​ 016/j.​
envpol.​2020.​115985
Onydinma UP, Aljerf L, Obike A, Onah OE, Caleb NJ (2021) Evalu-
ation of physicochemical characteristics and health risk of poly-
cyclic aromatic hydrocarbons in borehole waters around automo-
bile workshops in Southeastern Nigeria. Groundw Sustain Dev
14:100615. https://​doi.​org/​10.​1016/j.​gsd.​2021.​100615
Piveli RP (2015) Water quality and pollution: physical-chemical
aspects, 2nd. ed. [In Portuguese]
Prieto M, Cubillas P, Fernández-Gonzalez Á (2003) Uptake of dis-
solved Cd by biogenic and abiogenic aragonite: a comparison with
sorption onto calcite. Geochim Cosmochim Acta 67:3859–3869.
https://​doi.​org/​10.​1016/​S0016-​7037(03)​00309-0
Reyes-Torres M, Oviedo-Ocana E, Dominguez I, Komilis D, Sãnchez
A (2018) A systematic review on the composting of green waste:
feedstock quality and optimization strategies. Waste Manag
77:486–499. https://​doi.​org/​10.​1016/j.​wasman.​2018.​04.​037
Salo T, Salovius-Laurén S (2022) Green algae as bioindicators for long-
term nutrient pollution along a coastal eutrophication gradient.
Ecol Indic 140:109034. https://​doi.​org/​10.​1016/j.​ecoli​nd.​2022.​
109034
Sdiri A, Higashi T, Jamoussi F, Bouaziz S (2012) Effects of impurities
on the removal of heavy metals by natural limestones in aqueous
systems. J Environ Manage 93:245–253. https://d​ oi.o​ rg/1​ 0.1​ 016/j.​
jenvm​an.​2011.​08.​002
Silva D, Debacher NA, Junio ABC, Rohers F (2010) Physical-chemical
and microstructural characterization of bivalve mollusc shells
from cultivations in the coastal region of Santa Catarina Island.
Quím Nova 33(5):1053–1058. https://​doi.​org/​10.​1590/​S0100-​
40422​01000​05000​09. (In Portuguese)
Silva JRM, Oliveira LFC, Franco CS, Oliveira JE, Silvério BB (2021)
Adsorption of metal ions in red marine algae Lithothamnium cal-
careum in the treatment of industrial effluents. Rev Ambient Água
16(5):1–16. https://​doi.​org/​10.​4136/​ambi-​agua.​2740
Sondi I, Bišćan J, Vdović N, Škapin SD (2009) The electrokinetic
properties of carbonates in aqueous media revisited. Colloids Surf
A 342:84–91. https://​doi.​org/​10.​1016/j.​colsu​rfa.​2009.​04.​012
Sposito GA (1984) The surface chemistry of soils. Oxford University
Press: 1984.
Tchobanoglous G, Stensel HD, Tsuchihashi R, Burton F, Abu-Orf
M, Bowden G (2016) Pfrang W (2016) Wastewater engineering:
13

treatment and reuse, 5th edn. The McGraw-Hill Companies Inc,
New York
Ukaogo PO, Tang J, Ahuchaogu AA, Igwe OU, Obike AI, Emole PO,
Aljerf L, Onah OE, Tijjani A, Ajong AB (2022) Evaluation of
concentrations of trace metal(loid)s in indigenous crab species
and human health risk implications. Emerg Contam 8:371–380.
https://​doi.​org/​10.​1016/j.​emcon.​2022.​07.​001
Veneu DM (2017) Bioclastic Granules (Lithothamnium Calcareum) for
the removal of lead, cadmium or nickel from aqueous solutions.
[D.Sc. thesi] Rio de Janeiro: Federal University of Rio de Janeiro,
School of Chemistry. [In Portuguese]
Veneu DM, Schneider CL, Monte MBM, Cunha OGC, Yokoyama L
(2018) Cadmium removal by Bioclastic Granules (Lithothamnium
calcareum): batch and fixed-bed column systems sorption stud-
ies. Environ Technol 39(13):1670–1681. https://​doi.​org/​10.​1080/​
09593​330.​2017.​13365​74
Veneu DM, Yokoyama L, Cunha OGC, Schneider CL, Monte MBM
(2018) Nickel sorption using Bioclastic Granules as a sorbent mate-
rial: equilibrium, kinetic and characterization studies. J Mater Res
Technol 8(1):840–852. https://​doi.​org/​10.​1016/j.​jmrt.​2018.​05.​020
Veneu DM, Yokoyama L, Cunha OGC, Schneider CL, Monte MBM
(2017) Application of Bioclastic Granules (GB) for Ni(II) removal
from aqueous solutions. In: XXVII National Meeting of Ore
Treatment and Extractive Metallurgy; 2017 Oct 22–26; Pará,
Brazil, p. 2041–2048. [In Portuguese]
Vila GB (2012) Characterization of calcium silicates and carbonates
applied to high dose dosimetry. [D.Sc. thesi] São Paulo: Institute
for Energy and Nuclear Research; 2012. [In Portuguese]
Volschan Jr I (2022) Cause and effects of sewage pollution and the
water supply crisis in the Metropolitan Region of Rio de Janeiro.
Plurale [Internet] 2022; [cited 2022 feb 2] Available from: https://​
13
Environmental Science and Pollution Research
www.​plura​le.​com.​br/​site/​notic​ias-​detal​hes.​php?​cod=​17303​&​
codSe​cao=​11&​oMnu=​espec​iais&​sub=​agua [In Portuguese]
Wang X, Huang J, Huai Q, Wang J, Qin Y (2007) Determination of
kinetic and equilibrium parameters of the batch adsorption of
Ni(II) from aqueous solutions by Na-Mordenite. J Hazard Mater
142:468–476. https://​doi.​org/​10.​1016/j.​jhazm​at.​2006.​08.​047
Wu DY, Zhang BH, Li CJ, Zhang ZJ, Kong HN (2006) Simultaneous
removal of ammonium and phosphate by zeolite synthesized from
fly ash as influenced by salt treatment. J Colloid Interface Sci
304:300–306. https://​doi.​org/​10.​1016/j.​jcis.​2006.​09.​011
Wu B, Wan J, Zhang Y, Pan B, Lo IMC (2020) Selective phosphate
removal from water and wastewater using sorption: process funda-
mentals and removal mechanisms. Environ Sci Tecnol 54:50–66.
https://​doi.​org/​10.​1021/​acs.​est.​9b055​69
Zand AD, Abyaneh MR (2020) Adsorption of Lead, manganese, and
copper onto biochar in landfill leachate: implication of non-linear
regression analysis. Sustain Environ Res 30:18. https://d​ oi.o​ rg/1​ 0.​
1186/​s42834-​020-​00061-9
Zeng L, Johnson RL, Li X, Liu J (2003) Phosphorus removal from
aqueous solutions by sorption on two volcanic soils. Can J Soil
Sci 547–556. https://​doi.​org/​10.​4141/​S03-​006
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