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agronomy
Article
Speciation of P in Solid Organic Fertilisers from Digestate
and Biowaste
Inge C. Regelink 1, Caleb E. Egene 2, * , Filip M. G. Tack 2and Erik Meers 2
Citation: Regelink, I.C.; Egene, C.E.;
Tack, F.M.G.; Meers, E. Speciation of P
in Solid Organic Fertilisers from
Digestate and Biowaste. Agronomy
2021,11, 2233. https://doi.org/
10.3390/agronomy11112233
Academic Editor: Hans-Werner Olfs
Received: 14 September 2021
Accepted: 31 October 2021
Published: 4 November 2021
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1Wageningen Environmental Research, Wageningen University and Research (WUR), 6708 PB Wageningen,
The Netherlands; inge.regelink@wur.nl
2Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University,
Coupure Links 653, 9000 Ghent, Belgium; filip.tack@ugent.be (F.M.G.T.); erik.meers@ugent.be (E.M.)
*Correspondence: calebelijah.egene@ugent.be
Abstract:
Phosphorus (P) is a finite resource and its reuse in organic fertilisers made from biowaste
and manure should therefore be encouraged. The composition of solid organic fertilisers (SOFs)
depends on the type of feedstock and processing conditions, and this may affect P speciation and
hence P availability. Phosphorus speciation was assessed in eighteen different SOFs produced from
biowaste and digestate. Available P was determined in 10 mM CaCl
2
extracts at a fixed pH of 5.5 and
at a fixed total P concentration in the suspension. P was dominantly present as inorganic P (>80%
of total P). There was a strong variation in the Fe content of the SOFs and hence in the fraction of P
bound to reactive Fe/Al-oxides (P
Fe
). The fraction of total P soluble at pH 5.5 correlated negatively
with P
Fe
pointing to fixation of P by metal salts added during processing, or by soil mineral particles
in case garden waste was processed. Therefore, the use of iron salts in processing plants should be
avoided. In addition, the presence of P in poorly soluble precipitates lowered the fraction of easily
available P. Overall, this study shows that P
t
alone is not a good indicator for the agronomic efficiency
of SOFs due to large differences in P speciation among SOFs.
Keywords: manure; solid fraction of digestate; compost; phosphorus; iron salts
1. Introduction
Most of the phosphorus (P) used in agriculture today is derived from the mining of
nonrenewable phosphate rock. However, global P reserves are rapidly being depleted [
1
]
thus raising important questions about the long-term supply security of P [
2
]. Recovery
and recycling of P are vital for sustaining long-term food production as over 90% of current
P resources are used as fertilisers [
1
,
3
]. Biowaste from consumers and food processing
industries forms a large yet mostly unexploited resource of P [
4
]. Food waste is the second
largest flow of P losses in the EU after sewage sludge from communal wastewater treatment
plants [
4
]. Animal manure is another large resource of P which is, in areas with a surplus of
animal manure, often used in excess as compared to crop uptake resulting in accumulation
of P in soils and runoff to surface water [
4
]. Processing biowaste and manure into safe and
agronomically efficient fertilisers that can replace the current use of P fertilisers from fossil
resources is, therefore, essential.
Solid organic fertilisers (SOFs) include a wide array of biobased products that are
characterized by high organic matter contents and moderate to high amounts of organic
and/or inorganic P. Common SOFs typically used in agriculture include the solid fraction
(SF) of animal manure [
5
,
6
], raw or mechanically separated digestate from anaerobic di-
gestion (AD) of animal manure, energy crops and food waste [
7
–
9
], composts and garden
waste [
10
,
11
], among others. In practice, the choice of which SOF to use as a P source is
often based on their total P content. However, this may not be indicative of the plant-
available P content of the SOFs. The availability of P depends on its speciation, which
may vary among SOFs depending on feedstock composition and the type of processing
Agronomy 2021,11, 2233. https://doi.org/10.3390/agronomy11112233 https://www.mdpi.com/journal/agronomy
Agronomy 2021,11, 2233 2 of 18
treatments applied [
12
–
14
]. Since plants can only utilise P in inorganic form, speciation
and solubility of the inorganic P is most relevant in terms of plant-availability. Inorganic P
is often associated with multivalent cations forming phosphate salts including brushite
(CaHPO
4·
2H
2
O) and struvite (MgNH
4
PO
4·
6H
2
O) [
15
]. These precipitates typically dis-
solve under slightly acidic conditions thereby releasing orthophosphate (P-PO
4
) [
16
,
17
]. Of
particular importance are levels of Fe and Al in the SOF since P is preferentially bound to
these metals either through precipitation as, for example, vivianite (Fe
3
(PO
4
)
2·
8H
2
O) [
18
]
or through adsorption onto the surfaces of amorphous Fe and Al-oxides [
10
,
19
,
20
] thereby
controlling soluble P concentrations at a low level even under slightly acidic conditions.
Elevated concentrations of Fe or Al in the SFs of digestates have been linked to the addition
of Fe- or Al-based precipitating agents during feedstock processing [14,21] to control H2S
production [
22
] or to improve the separation efficiency for organic substances and P during
solid-liquid separation [
23
]. Additionally, the use of feedstocks containing high levels of
mineral particles, such as garden waste and iron-rich flotation sludges from industrial
wastewater treatment plants (WWTP), may contribute to high levels of Fe and Al in SOFs.
There is, therefore, a need to assess P speciation and levels of easily available P in SOFs,
and in particular in relation to Fe and Al contents.
Ammonium-oxalate (oxalate) extraction [
24
] is conventionally used to differentiate
between reactive pools of Fe, Al, and P (Al
ox
, Fe
ox
, and P
ox
, respectively) and the more
stable, nonreactive pools. Total Fe, for example, may represent multiple iron minerals
including structurally bound Fe in clay minerals, crystalline Fe-(hydr)oxides (e.g., goethite)
and amorphous Fe hydroxides (e.g., ferrihydrite), and these Fe minerals strongly differ
in terms of P binding capacity. Therefore, in order to assess the P binding capacity of a P
source, Fe
ox
and Al
ox
are more informative since the oxalate extraction procedure targets
only small and amorphous Fe and Al-(hydr)oxides with a high capacity for adsorption of
P. Similarly, P
ox
represents the P fraction that is associated with Fe/Al-oxides. However,
this assumption only holds for soils or organic products containing high amounts of soil
particles such as compost. It is worth noting that the P
ox
extraction method also extracts
acid-soluble P forms including struvite and calcium phosphate meaning that P
ox
may
overestimate the amount of P bound to Fe/Al-oxides in SOFs with a high P
ox
and low Fe
ox
content. This distinction is important since Fe
ox
, Al
ox
, and P
ox
concentrations are often
used as indicators for predicting P availability [25–28].
Earlier studies have evaluated different chemical extractions for predicting P avail-
ability in SOFs but results have been inconclusive for a variety of reasons. Elliot et al. [
29
]
assessed the use of neutral ammonium-citrate-soluble P (0.88 M citrate solution at 65
◦
C) to
estimate plant-available P in SOFs but found that it could not distinguish between directly
available P and P bound to Fe/Al-oxides due to dissolution of the latter metals. Meyer
et al. [
13
] found that a water extraction underestimated, while the citric acid extraction
overestimated, the plant-available P in recycled fertilisers. Janßen [
30
] criticized the use of
the CAT extraction method (10 mM CaCl
2
+ 2 mM DTPA) for determining easily available
P-PO
4
in soil improvers for being insensitive to small differences in the composition of
materials under investigation, which may lead to overestimation of the available P, es-
pecially in materials with high pH. The use of extraction solutions containing chelates
(e.g., citrate, DTPA) overestimates the fraction of easily available P due to the dissolution
of Fe/Al-oxides. This can be prevented by using a mild salt solution or demineralized
water as an extractant. For instance, extraction with 10 mM CaCl
2
has been widely used to
relate easily available P in SOFs [
31
,
32
] and SOF-amended soils [
33
–
36
] to plant-available P.
However, it was found that water-extractable P in compost decreased with increasing pH
due to the pH-dependent solubility of phosphate salts [36].
The issues related to the use of the aforementioned methods suggest that two im-
portant factors control their reliability when comparing P availability in SOFs. Firstly,
at the pH value of most SOFs (>7), the measured P-PO
4
concentration is the result of
the solubility products of Ca and/or Mg phosphate salts (calcium phosphate, struvite,
etc.). Composts and SFs of digestate usually have a slightly alkaline pH and this means
Agronomy 2021,11, 2233 3 of 18
that water-extractable P levels underestimate the fraction of available P when the SOF is
applied on a soil with a neutral or slightly acidic pH. Secondly, the methods adopt a fixed
mass:extractant ratio which means that large differences in total P content in the SOFs
are not accounted for. In that case, for SOFs with a higher P content, less P will go into
solution relative to total P under conditions where the P concentration in the extractant
is controlled by the solubility product of phosphate salts or by a desorption equilibrium.
Brod et al. [
37
] demonstrated that different SOFs, with different initial pH values, exert
varying degrees of influence on the pH of the extraction solution and this variation was
partly explained by mass:extractant ratio used in the extraction. Therefore, a more reliable
method for predicting the P fertilising potential of SOFs should consider the type of P
compounds present in the fertiliser as well as the pH of the target soil [23].
In practice, the application rate for P fertilisation is adjusted based on the total P
content of the SOFs. However, the proportion of P that will go into solution after application
is strongly influenced by the pH of the agricultural soil. Thus, we hypothesized that by
evaluating P availability based on a fixed total P content in the extraction solution and
at uniform pH, artefacts’ due differences in the P content and pH value of the SOFs will
be avoided. Furthermore, the proposed methodology will likely reveal new relationships
between available P and inherent SOF characteristics, which will make it possible to identify
indicators that can distinguish differences in P availability among SOFs.
The purpose of this study was to test a novel approach for assessing P speciation
in eighteen SOFs originating from diverse feedstocks and processing treatments with a
specific focus on the use of iron salts or iron-rich feedstocks. The second aim of the study
was to establish a relationship between easily available P (P-CaCl
2
) and other characteristics
of the SOF, including its Feox content.
2. Materials and Methods
2.1. Origin of the Solid Organic Fertilisers
In total, eighteen SOFs were collected (Table 1). Ten samples of SF of digestates were
obtained from six full-scale anaerobic digestion (AD) plants, six samples of composts and
three samples of sieved soils were collected from six biowaste treatment facilities.
Table 1. Origin of the solid organic fertilisers, feedstock and description of feedstock processing a.
Type Processing Plant Code Feedstock and Processing Fe-Salts d
SF of digestate
AM-Power bAMP-SF
Dried SF of digestate of biowaste
including incl. sludge from
agro-food industry
N
Groot Zevert Vergisting b
GZV-SF1 SF of digestate of pig manure and
biowaste N
GZV-SF2 Low-P SF obtained after leaching
P with water and sulphuric acid N
Benas b
BNS-SF1
SF of digestate of energy crops and
poultry litter N
BNS-SF2 Low N SF obtained by removing
N through stripping N
Waterleau New Energy b
WNE-SF1
Dried SF of digestate of manure
and biowaste incl. sludge from
agro-food industry
Y
WNE-SF2 Dried SF mixed with concentrated
liquid fraction of digestate Y
Dairy farm cDF-SF SF of digestate of dairy manure N
Sugar-beet processing
company BP-SF SF of digestate of residues from
sugar beets Y
Agronomy 2021,11, 2233 4 of 18
Table 1. Cont.
Type Processing Plant Code Feedstock and Processing Fe-Salts d
Compost Biowaste treatment
facilities
VFG-COMP1 Compost of source separated VFG
waste
N
VFG-COMP2 N
VFG-COMP3 Compost of digestate of source
separated VFG waste.
Y
VFG-COMP4 Y
GW-COMP1 Compost of garden waste N
GW-COMP2 N
Sieved soil Biowaste treatment
facilities
SOIL1 Fraction < 2 mm obtained by
sieving garden waste prior to
composting
N
SOIL2 N
SOIL3 N
a
SF: solid fraction, AMP: Am-Power, GZV: Groot Zevert Vergisting, BNS: Benas, WNE: Waterleau New Energy, APF: Arjan Prinssen Farm,
VFG-COMP: compost of vegetable, fruit and garden (VFG) waste, GW-COMP: compost of garden waste (GW).
b
Demonstration plants
within the H2020 project SYSTEMIC.
c
Demonstration plant within the H2020 project FertiManure.
d
Fe: the use of iron salts or iron water
in the digester or digestate processing facilities, Y; yes, N; no.
AM-Power (AMP, Pittem, Belgium) treats residues from the food processing industry
and source-separated food waste via thermophilic (~55
◦
C) AD with a retention time of
about 60 days. Iron salts are not added but the feedstock includes iron-rich sludge from
WWTPs of food processing companies. A decanter is used to separate the digestate into
solid and liquid fractions using polymers to improve separation efficiency. The SF is
thereafter dried at 60 ◦C in a fluidized bed dryer (AMP-SF).
Benas (BNS, Ottersberg, Germany) treats energy crops (silage maize, silage rye and
corn, 85% w/w) and poultry litter (15% w/w) using thermophilic digestion. The ammonia
content of the digestate is lowered through treatment of a side stream of digestate by
means of an N stripper to control inhibition of biogas formation resulting from ammonia
toxification. A screw press was used to separate the SF from the main digestate stream
(BNS-SF1). A second SF was collected from a screw press located immediately after the
N stripper resulting in a SF with a reduced N content (BNS-SF2). BNS-SF2 was air-dried
whereas BNS-SF1 was not dried.
Groot Zevert Vergisting (GZV, Beltrum, The Netherlands) operates a mesophilic
(~35
◦
C) AD plant that is fed with pig slurry (81% w/w) and food processing residues (a.o.
grain and rice husk, potato skins and coffee grounds, 19% w/w). Digestate is dewatered
through a decanter (GZV-SF1) without the use of additives. Part of the SF is further
processed in an installation to remove and recover P which includes washing the SF
with water and sulphuric acid to obtain a SF with a reduced P content and a fibrous
structure (GZV-SF2).
Waterleau New Energy (WNE, Ieper, Belgium) operates an AD plant used for the
mesophilic (~35
◦
C) digestion of residues from agroindustry (potatoes and grain, 40% w/w),
sludge from industrial WWTPs (15% w/w) and animal manure (45% w/w). Digestate is
passed through a decanter to obtain a SF which is thereafter dried producing a solid organic
fertiliser (WNE-SF). Iron sludge (a side product from drinking water production) and FeCl
3
salts are added in the AD and during the separation process to bind H
2
S and to improve
the separation efficiency. The liquid fraction of the digestate was further processed by
means of reverse osmosis and evaporation and the N + K-rich evaporator concentrate was
mixed with the dried SF producing a paste-like product (WNE-SF2). WNE, GZV, AMP and
BNS are demonstration plants within the EU project SYSTEMIC and more information is
available on [38] and in Brienza et al. [39].
The dairy farm (DF, Haarlo, The Netherlands) processes dairy manure (90% w/w)
and coproducts (beet tips and grass, 10% w/w) in a mesophilic (~35
◦
C) AD followed by
N stripping and solid-liquid separation using a screw press without the use of chemical
Agronomy 2021,11, 2233 5 of 18
additives. The SF is referred to as DF-SF. This dairy farm is a demonstration plant within
the EU project FERTIMANURE [40].
A sugar beet processing company treats residues from sugar beets (beet tips and beet
pulp) in a mesophilic AD plant. Iron sludge (a residue from the production of drinking
water from groundwater) was added to control H
2
S emissions and digestate was dewatered
by a decanter (BP-SF).
Four compost samples originated from source-separated vegetable fruit and garden
(VFG) waste which are here referred to as VFG-COMP1&2 and VFG-COMP3&4 where
the latter refers to the two plants where VFG waste is digested before composting leading
to elevated Fe contents due to the addition of Fe salts during digestion to control H
2
S
emissions. Two composts were produced from garden waste (GW) and are referred to as
GW-COMP1 and GW-COMP2.
Three samples of sieved soil were collected from biowaste treatment companies.
Sieved soil is defined as the <2 mm fraction obtained after sieving garden waste to separate
the soil fraction from the organic material. Sieved soils are typically not considered as
fertiliser but are included in this study as reference material to compare the availability of
P in organic fertilisers with high amounts of soil fraction in organic waste.
2.2. Analytical Methods
2.2.1. Solid Organic Fertiliser Characterisation
About 10 kg of fresh material was homogenized, dried at 40
◦
C, ground and sieved
over 2 mm and hereafter referred to as ‘dried samples’. About 5 kg of fresh material
was stored in a fridge until analyses. Dry weight (DW) was determined of fresh samples
after drying at 105
◦
C for 24 h. The OM content was determined on dried samples by
loss-on-ignition at 550
◦
C. Total contents of P, Ca, Mg, K, S and Fe (P
t
, Ca
t
, Mg
t
, K
t
and S
t
)
were determined after destruction of dried sample by the aqua regia method followed by
analysis of the elemental concentrations using inductively coupled plasma optical emission
spectroscopy (ICP-OES) [
41
]. Total N was determined using the Kjeldahl method [
42
]. pH
was determined by extracting fresh samples with 10 mM CaCl
2
using a 1:10 (w/v) sample
to extractant ratio [43].
2.2.2. P Extraction Procedures
An overview of the P-pools evaluated in this study and their respective methods is
given in Table 2. The P
t-kuo
method [
44
] was used to distinguish between inorganic P (P
io
)
and organic P (P
o
). Inorganic P was determined by extracting 2 g of dried sample with
50 mL of 0.5 M H
2
SO
4
followed by shaking for 16 h, filtration over 0.45
µ
m and colorimetric
measurement of P-PO
4
in the filtrate. Total P (P
t,kuo
) was determined after oxidation of
the sample at 550
◦
C followed by extraction with 0.5 M H
2
SO
4
and P
o
was defined as the
difference between Pt,kuo and Pio.
Oxalate-extractable P, Fe and Al (P
ox
, Fe
ox
, Al
ox
) were determined by shaking 1 g
of dried sample with 0.2 M ammonium oxalate at pH 3.0 for 4 h in the dark followed
by centrifugation, filtration (0.45
µ
m) and analyses of the filtrate on P, Fe and Al by ICP-
OES [45].
Easily available P was determined using an adapted CaCl
2
extraction procedure using
a predetermined P
t
content in the suspension of 150 mg P/L. An amount of fresh sample
containing 75 mg P was added to 500 mL 10 mM CaCl
2
solution and horizontally shaken
for 30 min. Fresh samples were used to prevent artefacts due to drying. The fixed P
t
content
prevent artefacts due to strong differences in P
t
between samples. The sample to extraction
ratio varied between 6–100 g/L based on DW. After 30 min of shaking, a 30 mL subsample
was taken, centrifuged and filtrated (0.45 um membrane filter). The remaining suspension
(470 mL) was thereafter put in a 1 L beaker glass and stirred using a magnetic stirrer while
0.8 M H
2
SO
4
was added to decrease the pH to 5.0. Once a stable pH was reached, the
suspensions were stirred for another 30 min and thereafter sampled as described above.
During the 30 min of shaking, pH slightly increased towards values between 5.5 and 5.8.
Agronomy 2021,11, 2233 6 of 18
All filtrates were analysed on P-PO
4
, N-NH
4
and N-NO
3
and dissolved organic carbon
(DOC) (spectrophotometrically using a segmented flow analyser) and on total P, Ca, Mg, K,
P, Fe and Al by ICP-OES (Thermo Fisher Scientific, iCAP 6500 duo, Waltham, MA, USA).
Total P in CaCl
2
is referred to as P-CaCl
2
(at the initial pH) and P-CaCl
2,pH5
.
5
(at pH 5.5).
Organic P in the CaCl
2
-extracts is defined as the difference between total P (ICP-OES) and
P-PO
4
. The CaCl
2
extraction was performed in duplicate on five out of the 18 samples to
check the reproducibility of the method. Results of the P-CaCl
2
-extractions are reported as
% of total P that has been dissolved, which was logical because of the fixed total P level in
the suspensions. For P-CaCl
2
(initial pH), difference between duplicates was <0.7% of P
total (absolute difference). For P-CaCl
2,pH5
.
5
values, relative differences between duplicates
was less than 15% (relative difference).
Table 2.
Overview of the P pools and associated analytical methods used to assess P speciation in the solid organic fertilisers.
Name P-Pool Analytical Method
PtTotal P P soluble after destruction with aqua regia
Pt,kuo Total P P-PO4extracted with 0.5 M H2SO4after oxidation at
550 ◦C
Pio Total inorganic P P-PO4soluble in 0.5 M H2SO4
PoTotal organic P Difference Pt,kuo and Pio
Pox P associated with Fe- and Al-oxides, acid-soluble P
salts and a part of the organic P
P extracted in acid ammonium-oxalate, measured as
total P (ICP-OES)
P-CaCl2Directly available P without pH adjustment
P extractable in 10 mM CaCl
2
using fresh material and
at a predetermined total P concentration of 150 mg/L
in the suspension a
P-CaCl2 (pH5.5) Easily soluble P at pH 5.5 As P-CaCl2but after lowering the pH of the
suspension to 5.0 (at equilibrium, average pH was 5.5)
a
The method differs from the standard P-CaCl
2
-extraction approach for soils which uses a fixed soil to solution ratio of 0.1 kg/L. Here, a
fixed total amount of P/L of extractant was used to prevent artefacts due to the wide range of P-contents in organic fertilisers.
2.3. Data Analysis
Statistical analyses were performed using IBM SPSS Statistics software (version 23).
Simple or multiple linear regression analyses were carried out to evaluate the relationships
between some of the variables across all treatments. The strength of the correlations
was reported using the coefficients of determination (R
2
). All tests were carried out at a
significance level of α= 0.05.
3. Results and Discussion
3.1. General Composition
There is a large variation in the composition of the studied SOFs (Table 3) which was
attributed to the differences in their feedstocks and processing treatments (Table 2). Dry
weight varied considerably between the SFs of digestate (23 to 95%) depending on the
type of dewatering equipment used and whether a drying step was included on the plant.
The OM content on DW basis was highest in the SFs of digestate (46% to 93%), low to
moderate in the composts (16–44%), and lowest in the sieved soils (11–21%). Among the
SFs, AMP-SF and BP-SF showed the lowest OM contents on DW basis with 46% and 49%,
respectively. These low OM values, which were similar to those measured in the composts,
coincide with the highest Fe contents (35 and 20 g/kg DW, respectively), and this may
point to the addition of iron salts during the process and/or the presence of significant
amounts of mineral particles in the feedstock i.e., garden waste, crop residues or iron-rich
sludges used in the anaerobic digester. The pH of the SFs of digestate and composts varied
between 7.0 and 8.7, which fell within the normal range for such organic products [
46
–
48
],
except for the SF with reduced P content (GZV-SF2) which had a slightly acidic pH of
Agronomy 2021,11, 2233 7 of 18
5.5 due to treatment with sulphuric acid. Alkaline pH in digestates and compost may
induce precipitation of phosphates with Ca and Mg to form (poorly water-soluble) calcium
phosphate and struvite compounds [49].
Table 3.
Composition of the studied solid fractions (SF’s) of digestate, composts (COMP) and sieved soils (soil) expressed
on dry weight (DW) a, b.
Sample DW OM pH-CaCl2PtNtKtMgtCatStFetFeox Alox Feox/FetPt/OM
% % of DW - g/kg DW - g/kg
AMP-SF 80 46 8.6 28 18 16 11 32 17 35 25.9 1.4 0.74 60
WNE-SF1 95 65 8.1 26 28 22 11 49 13 13 9.6 0.5 0.73 39
WNE-SF2 56 62 7.9 23 31 51 9.7 41 19 11 8.4 0.4 0.74 38
GZV-SF1 31 76 8.7 28 38 16 19 30 6.5 2.8 2.4 0.2 0.86 37
GZV-SF2 23 93 5.0 3.8 14 <1.0 2.1 9.6 10 2.3 1.6
<0.05
0.69 4.1
BNS-SF1 25 91 8.7 6.2 34 23 3.4 7.0 3.9 5.5 4.5
<0.05
0.81 6.8
BNS-SF2 66 92 7.1 4.7 12 16 2.9 8.3 4.2 5.5 4.4
<0.05
0.80 5.1
BP-SF 33 49 8.4 5.1 26 14 4.8 64 9.8 20 15.2 0.3 0.76 10
DF-SF 26 79 7.1 12 25 29 12 26 7.5 2.6 1.8 0.1 0.69 15
VFG-
COMP1 69 41 7.8 3.4 16 13 4.8 35 2.9 11 2.0 0.3 0.18 8.2
VFG-
COMP2 69 43 7.6 3.5 15 9.6 3.7 32 6.6 5.0 1.7 0.7 0.35 8.1
VFG-
COMP3 60 35 8.0 2.6 14 9.1 3.6 23 2.1 7.3 2.4 0.6 0.33 7.5
VFG-
COMP4 67 44 7.5 3.1 18 13 4.5 30 2.6 11 4.6 0.5 0.41 7.1
GW-
COMP1 42 39 7.9 1.5 7.9 7.0 2.9 24 1.1 10 2.7 0.3 0.27 4.0
GW-
COMP2 67 16 7.0 1.1 6.0 3.8 1.9 8.8 1.5 8.6 3.0 0.6 0.35 6.7
Soil1 70 21 6.9 1.3 7.0 4.6 1.7 12 1.1 6.3 2.5 0.7 0.39 6.2
Soil2 75 11 6.8 0.8 3.6 1.8 1.4 8.6 0.6 5.1 2.6 0.8 0.50 7.4
Soil3 66 18 6.7 0.8 3.9 1.7 1.1 5.8 0.5 4.5 2.3 0.9 0.52 4.3
a
DW: dry weight: OM: organic matter. SF: Solid fraction, AMP: Am-Power, GZV: Groot Zevert Vergisting, BNS: Benas, WNE: Waterleau
New Energy, APF: Arjan Prinsen Farm, VFG-COMP: compost of vegetable, fruit and garden (VFG) waste, GW-COMP: compost of garden
waste (GW).
b
Total amounts of P, Ca, Mg, K, S and Fe after destruction with aqua regia. Fe-ox and Al-ox determined after extraction with
acid ammonium-oxalate/oxalic acid.
P
t
contents varied widely between and within the product types. The SFs of digestate
contained between 3.8–28 g P/kg DW, with the lowest P
t
in the SF that underwent P
recovery (GZV-SF2) and the highest in the SF from GZV without P recovery (GZV-SF1).
Differences in P
t
contents of the SFs were due to differences in digester feedstock, with
rather low P
t
contents in SFs produced from digestate of energy crops (BNS-SF1&2) and
beet pulp (BP-SF) and high P
t
contents in SFs from biowaste (AMP-SF) or co-digested
pig manure (WNE-SF1&2 and GVZ-SF1). An exception was GZV-SF2 in which the P
t
content was reduced by nearly 90% after the post-treatment step in which the SF (GZV-
SF1) was leached with water and sulphuric acid at a pH of 5.0. This process, which is
running at full scale at GZV, is referred to as the RePeat process and described in more
detail elsewhere [
39
]. The VGF composts contained low P
t
contents ranging from 2.6 to
4.0 g P/kg DW while lower values were found in GW compost (1.1–1.5 g/kg DW) and
the sieved soils (
0.8–1.3 g/kg DW
). However, the actual amount of P that will be made
available to plants depends on the level of extractable or bioavailable P rather than on the
total P content.
Agronomy 2021,11, 2233 8 of 18
The P
t
/OM ratio, which is a determinant for the amount of P added to the soil per unit
of OM, varied widely and more so in the SFs of digestate (4–60 g/kg) than in the composts
(4–8 g/kg) and soils (4–7 g/kg) (Table 3). SOFs with high P
t
/OM ratios should primarily
be considered as P fertilisers whereas SOFs with low P
t
/OM ratios can be considered
primarily as organic soil improvers. There is no clear distinction between a P fertiliser and
an organic soil improver, but in general, an SOF with a P
t/
OM ratio of 10 g/kg or lower
can be considered as organic soil improvers because they enable a farmer to apply about
2500 kg of organic matter without exceeding the yearly average P uptake or arable crops
(roughly 25 kg P/ha) [
50
]. Using this criterion, composts can be considered as organic soil
improvers fractions as well as those SFs that have low P
t
/OM ratios such as GZV-SF2, in
which P has been removed by means of acid, and the BNS-SF1&2 which originate from
digestate of energy crops. Sieved soils are also characterised by P
t
/OM ratios below 10,
however, sieved soil should be considered as soil rather than as organic soil improver
because of its low OM content (<21% of DW).
Similar to P
t
, total concentrations of N, K, Mg, Ca and S showed great variation in the
SOFs (Table 3). Nitrogen content varied between 12 and 34 g/kg DW in SFs of digestate and
was influenced by the processing of the digestate. Thermal drying (AMP-SF), ammonia
stripping (BNS-SF2) and leaching with acid (GZV-SF2) generally resulted in lower N
contents as compared to SFs from digestate that had not undergone such a treatment to
remove nitrogen from the solid fraction. Nitrogen contents of compost samples varied
between 7 and 16 g/kg which is somewhat lower as compared to the SFs. However, in
terms of agronomic efficiency, the N mineralisation rate is the factor determining nitrogen
availability from SOFs. N/P ratios in composts and SFs of digestate varied between 0.7
and 6.0 kg/kg. Assuming an N mineralisation coefficient of 10% for composts and 55% for
SFs of digestate [
47
], the effective N/P ratio is <2 kg/kg, with the exception of the low-P
product (GZV-SF2). Hence, the effective N/P ratio of the SOFs under investigation is low
as compared to the N/P crop requirements [
51
] and this further confirms that all tested
products should primarily be regarded as P fertilisers or organic soil improvers rather than
as N fertilisers.
3.2. Total and Reactive Fe
Total iron (Fe
t
) in the SOFs varied between 2.6 and 35.2 g/kg DW (Table 3). Among
the SFs of digestate, Fe
t
was highest in fertilisers produced by companies that add Fe salts
or treat Fe-rich feedstocks such as flotation sludges from the food industry (AMP, BP and
WNE). When no Fe was added, Fe
t
in SFs was below 5.5 g/kg DW. In the VFG-composts,
Fe
t
varied between 5.0 and 11.4 g/kg DW and was similar to Fe
t
in GW-compost and
only slightly higher as compared to Fe
t
in sieved soils (4.5–6.3 g/kg DW). There was
no difference in Fe
t
content between composts from treatment plants where VFG-waste
was anaerobically digested with Fe-salts (VFG-COMP3&4) and composts that did not
receive Fe-salts during processing (VFG-COMP1&2). Composts consist of more than 50%
of mineral particles, mostly soil particles, and differences in Fe
t
content between composts
are most likely due to differences in the mineralogy of the mineral soil fraction.
The Fe
ox
content is regarded as an indicator for the reactive Fe-oxides in the SOFs.
Though Fe
ox
correlated with Fe
t
(R
2
: 0.89, p< 0.01), there are distinct differences in the
Fe
ox
/Fe
t
ratio between product groups. The average Fe
ox
/Fe
t
ratio was high in SFs
of digestate (0.76
±
0.06) as compared to the composts (0.31
±
0.08) and sieved soil
(
0.46 ±0.07
) which points to differences in the origin of Fe between these product groups.
Low Fe
ox
/Fe
t
ratios in composts and sieved soils point to the presence of Fe in crystalline
minerals such as goethite or clay minerals that do not dissolve in the acid oxalate extraction
medium. On the other hand, Fe
ox
/Fe
t
is >0.70 in all SFs of digestate regardless of whether
Fe salts were added during processing. This points to Fe being dominantly present in the
reactive form due to its association with organic matter or presence of extractable minerals
including ferrihydrite (Fe
2
O
3·
0.5H
2
O), iron sulfide (Fe(II)S), strengite (Fe(III)PO
4·
2H
2
O)
Agronomy 2021,11, 2233 9 of 18
and vivianite (Fe(II)(PO
4
)
2·
8H
2
O) [
18
]. This also underscores that Fe
ox
rather than Fe
t
should be used as an indicator for determining the P binding capacity of SOFs.
Al
ox
contents were low compared to Fe
ox
contents and not distinctive for sieved
soils, compost or SFs of digestate (Table 3). Al
ox
contents were below the detection limit
(0.05 g/kg) in SFs of digestate from AD plants which were dominantly fed with animal
manure (GZV, APF) or energy crops (BNS) and higher in SOFs that include garden waste or
crop residue that may contain mineral soil particles such as beet tips and potato peels. Al
ox
decreased with increasing OM content (R
2
= 0.510, p< 0.01) regardless of product type. We,
therefore, argue that Al
ox
mostly originates from the mineral fraction associated with the
feedstock which explains the negative correlation between Al
ox
and OM. Such a correlation
with OM was not found for Fe
ox
and Fe
t
since Fe can enter SOFs either as a constituent of
soil particles, through the addition of Fe salts or from the treatment of Fe-rich sludges.
Overall, this points to a dominant role of mineral soil particles in determining levels
of Fe and Al in composts and sieved soils whereas Fe levels in SFs of digestate are related
to the use of Fe-salts or treatment of wastewater sludges containing precipitated Fe-salts.
3.3. Inorganic and Organic P
Inorganic P, defined as P extractable in 0.5 M H
2
SO
4
, was the dominant fraction in all
SOFs representing 65–101% of P
t
. Hence, only a small fraction of P
t
was present in organic
form (<24%) and this was not distinctive for the different product types. Similarly, other
authors found that only a small fraction of P
t
was present as organic P in composts and
digestates from manure and biowaste [10,52].
The total P content after dry combustion and extraction (P
t,kuo
) was on average 10%
lower as compared to the P
t
content determined by wet digestion. Other researchers found
that dry combustion followed by extraction of P in 0.5 M H
2
SO
4
slightly underestimated P
t
which was attributed to incomplete oxidation of OM, volatilization of P and formation of
insoluble P crystals during dry combustion at 550
◦
C [
53
,
54
]. It is also known that artefacts
may occur in the determination of the inorganic P fraction including hydrolysis of organic
P during the extraction of the inorganic P which, in turn, also affects the calculated organic
P content [54].
P
ox
contents, extracted with acid ammonium-oxalate, were similar to amounts of
inorganic P extracted with 0.5 M H
2
SO
4
(R
2
: 0.99, P < 0.01) indicating that despite the
differences in extraction medium, both analytical methods likely extracted the same P pool
from the SOFs. P
ox
made up 61–87% of P
t
. In soil science, P
ox
is regarded as the amount of
P adsorbed to amorphous Fe- and Al-oxides and, in combination with the Fe
ox
and Al
ox
content, used to calculate the degree of P saturation of the oxides in the soil [
55
]. However,
when applied to SOFs, P
ox
may seriously overestimate the amount of P adsorbed to Fe- and
Al-oxides because the acid oxalate extraction solution also dissolves commonly present
phosphate precipitates such as struvite and brushite (CaHPO
4·
2H
2
O) [
56
,
57
]. Hence, a
more sophisticated calculation is needed to derive the amount of P bound to Fe-oxides
in SOFs.
3.4. P Associated with Fe/Al-Oxides
The degree of P saturation (DPS) of the Fe/Al-oxides in SOF’s can be calculated with
Equation (1);
DPS (−)=Pox
0.5 ×(Feox +Alox)(1)
in which P
ox
, Fe
ox
and Al
ox
are expressed in mmol/kg. The factor 0.5 refers to the maximum
amount of P that can be bound to Fe/Al-oxides and has been derived for noncalcareous
sandy soils [
58
]. It may, however, underestimate the P binding capacity in case Fe and P
have precipitated to form vivianite (Fe
3
(PO
4
)
2·
8H
2
O) which has a molar P/Fe ratio of 2:3
and forms under anaerobic conditions [18].
The DPS approach was originally developed to predict P leaching in soils [
59
] but was
also successfully applied to predict P leaching from SOFs [
12
,
21
]. Elliot et al. [
12
] applied
Agronomy 2021,11, 2233 10 of 18
this approach to biosolids with high levels of Fe
ox
as compared to P
ox
and showed that a
DPS > 1 corresponded to an increased risk for P leaching from the biosolids. In our study,
DPS values of SFs of digestate and VFG compost were all above one except for the SF-BP
where iron was added during processing (Table 4). Sieved soil and GW compost had DPS
values below one meaning that Fe/Al-oxides are not fully saturated with P.
Table 4.
Percentage distribution of total P (P
t
) over the distinguished P species as well as the degree of P saturation (DPS) of
the Fe/Al oxides a.
Sample bInorganic P Organic P Pox P-CaCl2P-
CaCl2,pH5.5DPS PFe
% of Pt(-) % of Pt
AMP-SF 97 0.0 87 1.2 21 3.0 29
WNE-SF1 90 4.6 79 1.5 37 6.9 12
WNE-SF2 86 1.7 84 2.3 33 7.6 11
GZV-SF1 75 0.6 74 2.1 87 27 3
GZV-SF2 75 5.9 74 40 40 6.6 11
BNS-SF1 89 1.5 84 2.0 45 4.2 20
BNS-SF2 65 23 74 2.9 26 2.9 26
BP-SF 65 18 61 1.2 14 0.7 87
DF-SF 75 5.6 80 8.3 45 17 5
VFG-COMP1 76 8.5 62 0.4 18 2.8 22
VFG-COMP2 86 9.5 74 4.9 22 3.0 25
VFG-COMP3 89 8.1 71 0.6 22 1.8 39
VFG-COMP4 83 20 71 0.9 15 1.4 50
GW-COMP1 69 21 55 0.5 13 0.9 55
GW-COMP2 70 22 61 0.3 2 0.6 61
Soil1 76 13 64 0.4 6 0.7 64
Soil2 63 18 64 0.1 1 0.4 64
Soil3 65 22 64 0.2 1 0.4 64
a
P
t
: total P. Inorganic P: determined after extraction with 0.5 M H
2
SO
4
. Organic P: difference between P
t,kuo
(P extracted after dry
combustion followed by extracting with 0.5 M H
2
SO
4
) and inorganic P. P
ox
: P extracted in acid ammonium oxalate. P-CaCl
2
: P-PO
4
extracted with 10 mM CaCl
2
at a fixed total P concentration in the suspension of 150 mg P/L. P-CaCl
2,pH 5
.
5
: as P-CaCl
2
but at a pH of the
suspension of 5.5. DPS: degree of P saturation (Equation (1)). P
Fe
: P bound to Fe/Al oxides based on the P binding capacity of the organic
fertiliser, calculated using Equations (2) and (3).
b
SF: solid fraction, AMP: Am-Power, GZV: Groot Zevert Vergisting, BNS: Benas, WNE:
Waterleau New Energy, DF: dairy farm, VFG-COMP: compost of vegetable, fruit and garden (VFG) waste, GW-COMP: compost of garden
waste (GW).
The amount of P bound to Fe/Al-oxides can be calculated using the DPS to differenti-
ate between saturated and nonsaturated conditions. If the DPS is above one, and hence
the Fe/Al-oxides are saturated, the amount of P bound to Fe/Al-oxides is equal to the P
binding capacity (PBC) and can be calculated with Equation (2);
PFe g
kg =PBC =0.5 ∗(Feox +Alox)×31 ×1000 (if DPS >1)(2)
in which P
Fe
is the amount of P bound to Fe/Al-oxides and expressed in g/kg DW whereas
Fe
ox
and Al
ox
are in mmol/kg DW. The criteria of DPS > 1 is true for all SFs of digestates
and VFG-composts.
Agronomy 2021,11, 2233 11 of 18
If the DPS is below one, meaning that Fe/Al-oxides are not fully saturated with P, P
Fe
is assumed to equal Pox and Equation (3) is valid;
PFe g
kg =Pox ×31 ×1000 (if DPS <1)(3)
Table 4gives P
Fe
expressed as a percentage of P
t
. In the SFs, between 3 to 29% of P
t
is
bound to Fe/Al-oxides except for SF-BP in which 87% of P
t
was bound to Fe/Al-oxides. In
GW composts and sieved soil, the majority of P
t
is bound to Fe/Al-oxides (22–64% of P
t
)
whereas the VFG composts are in between SFs of digestate and GW composts (Table 4).
3.5. Easily Available P
The determination of P-CaCl
2
is relevant when assessing P release and availability
in SOFs [
33
,
34
] or soils [
31
,
60
]. Easily available P was determined after extraction of fresh
SOF with 10 mM CaCl
2
using a fixed P
t
concentration of 150 mg/L in the suspension. Fresh
samples were used since it is known that oven drying of manure and soil increases levels
of easily soluble P in manure [61] and soil samples [62].
Without pH adjustment, P extractable in CaCl
2
was low and corresponded to 0–8% of
P
t
except for GZV-SF2 in which 40% of P
t
was extractable in CaCl
2
. The latter SF had a pH
of 5.0 due to the treatment it had undergone to remove P. In the other SFs and composts,
pH values ranged between 7.0 and 8.6 implying that P-CaCl
2
is, in fact, controlled by the
equilibrium product of phosphate precipitates such as struvite and brushite (Table S1).
It was, therefore, concluded that P-CaCl
2
is unsuitable as an indicator for P availability
in the studied SOFs due to the predominant influence of the SOF’s pH. This leads to an
underestimation of available P when the pH of the SOF is high compared to the pH of the
soil to which the SOF is added.
Lowering the pH of the CaCl
2
suspensions led to, on average, a sevenfold increase in
the average P concentration in the CaCl
2
extracts. The pH-values of the suspensions were
initially lowered to 5.0, however, the pH slowly increased during the 30-min shaking period
leading to an average pH-value of 5.7
±
0.15 (Table S2) upon sampling and indicating
that controlling and maintaining pH-values is difficult and laborious. The fraction of
P-CaCl
2,pH5
.
5
extracted in the acidified CaCl
2
extracts was distinguishable for the different
product types. In SFs of digestate, 14–87% of P
t
was extracted at pH 5.5 which was
considerably higher as compared to the fraction extracted from composts (13–22%) and
sieved soils (1–6%) (Table 4). At the lowered pH, three mechanisms were predominant.
Firstly, precipitated phosphates which are insoluble at the pH of the SOFs (mean pH
≈
7.8), are released into solution. This was evidenced by the concomitant increase in
concentrations of PO
43−,
Mg
2+
and NH
4+
in ratios of 0.8 and 0.7 mol per mol of PO
43−,
respectively (Figure 1). In addition to struvite, calcium phosphate minerals such as brushite
may have been dissolved as well, but the change in Ca could not be determined due to the
10 mM CaCl
2
background provided by the extracting solution. The second mechanism
is the increased adsorption of P to reactive surfaces of Fe/Al-oxides at slightly acidic
pH values [
63
,
64
] and consequently, the saturation of Fe/Al-oxide binding sites with
phosphate ions. Using an even lower pH value, though, e.g., a pH value <4.0, would
lead to the dissolution of Fe-oxides and hence the release of associated P [
63
] and result in
an overestimation of P release upon addition of the SOFs to non-calcareous agricultural
soils. As such, the extraction at pH 5.5 targeted only the easily available P fraction that
would also be released upon addition of the SOF to a non-calcareous agricultural soil
which typically has a pH value of 5.0 to 6.0. Lastly, acidification of the CaCl
2
suspensions
caused a small increase in concentrations of organic P in the CaCl
2
extracts. On average,
18% of CaCl
2,pH5
.
5
was present in organic form (Table S2) and the organic P concentration
increased upon acidification of the CaCl
2
suspension. This is explained by the dissolution
and release of acid-labile organic P into solution [65].
Agronomy 2021,11, 2233 12 of 18
Agronomy 2021, 11, x FOR PEER REVIEW 12 of 18
Figure 1. Increase in the molar concentration of Mg or NH
4
(y-axis) plotted against the change in
PO
4
(x-axis) upon lowering the pH of the CaCl
2
suspensions towards pH 5.0 as compared to the
initial pH of the CaCl
2
suspensions. Lines are linear regression lines.
Figure 2a shows the relationship between P-CaCl
2,pH5.5
and P
Fe
, which are both ex-
pressed as % of P
t
, and shows a strong negative correlation between the two parameters
(R
2
: 0.70, p < 0.01). In SOFs where 50% or more of P
t
is bound to Fe/Al-oxides, less than
20% of P
t
is extractable in CaCl
2
at pH 5.5 which can be explained by the fact that P bound
to Fe/Al-oxides does not dissolve in the CaCl
2
at pH 5.5. The relationship between P-CaCl
2
(pH5.5)
and P
Fe
shows that P
ox
, Fe
ox
, and Al
ox
concentrations are useful measures for predict-
ing the P fertilising potential of SOFs in slightly acidic soils.
Multiple linear regression revealed that the OM content may also be a quick and sim-
ple indicator for available P in SOFs as a significant and positive relationship (R
2
= 0.59, p
< 0.01) was found between P-CaCl
2 (pH5.5)
and OM content (Figure 2b). In other words, SOFs
with high OM content released more P-CaCl
2
under acidified conditions. However, there
is no causal relation between the two parameters since the correlation is an effect of the
positive correlation between OM content and P
Fe
(R
2
: 0.78, p < 0.01). As a consequence, the
reliability of OM as an indicator for the easily available P fraction may be limited when
this relation is applied to other SOFs because (i) the relation was derived on a limited
number of samples and (ii) it can be expected that the reliability of OM as an indicator
decreases in samples in which the iron content is strongly influenced by the dosage of iron
salts during the processing process.
Figure 2. The relationships between P-PO
4
(% of Pt) measured in 10 mM CaCl
2
extracts (at initial pH and after acidification
to pH 5.5) and (A) the percentage of P bound to Fe/Al-oxides (P
Fe)
(B) organic matter content (%DW) in the organic ferti-
lisers.
y = 0.03x
R² = 0.02
y = -0.78x + 51.79
R² = 0.71
0
15
30
45
60
75
90
0 10203040506070
P-PO
4
(% of P
t
)
PFe (%)
P-CaCl2
P-CaCl2,pH5.5
Linear (P-CaCl2)
Linear (P-CaCl2,pH5.5)
A
y = 0.09x
R² = 0.31
y = 0.60x - 5.83
R² = 0.59
0
15
30
45
60
75
90
0 102030405060708090100
P-PO
4
(% of P
t
)
OM (% of DW)
B
Figure 1.
Increase in the molar concentration of Mg or NH
4
(y-axis) plotted against the change in
PO
4
(x-axis) upon lowering the pH of the CaCl
2
suspensions towards pH 5.0 as compared to the
initial pH of the CaCl2suspensions. Lines are linear regression lines.
Figure 2A shows the relationship between P-CaCl
2,pH5
.
5
and P
Fe
, which are both
expressed as % of P
t
, and shows a strong negative correlation between the two parameters
(R
2
: 0.70, p< 0.01). In SOFs where 50% or more of P
t
is bound to Fe/Al-oxides, less
than 20% of P
t
is extractable in CaCl
2
at pH 5.5 which can be explained by the fact that P
bound to Fe/Al-oxides does not dissolve in the CaCl
2
at pH 5.5. The relationship between
P-CaCl
2 (pH5
.
5)
and P
Fe
shows that P
ox
, Fe
ox
, and Al
ox
concentrations are useful measures
for predicting the P fertilising potential of SOFs in slightly acidic soils.
Agronomy 2021, 11, x FOR PEER REVIEW 12 of 18
Figure 1. Increase in the molar concentration of Mg or NH
4
(y-axis) plotted against the change in
PO
4
(x-axis) upon lowering the pH of the CaCl
2
suspensions towards pH 5.0 as compared to the
initial pH of the CaCl
2
suspensions. Lines are linear regression lines.
Figure 2a shows the relationship between P-CaCl
2,pH5.5
and P
Fe
, which are both ex-
pressed as % of P
t
, and shows a strong negative correlation between the two parameters
(R
2
: 0.70, p < 0.01). In SOFs where 50% or more of P
t
is bound to Fe/Al-oxides, less than
20% of P
t
is extractable in CaCl
2
at pH 5.5 which can be explained by the fact that P bound
to Fe/Al-oxides does not dissolve in the CaCl
2
at pH 5.5. The relationship between P-CaCl
2
(pH5.5)
and P
Fe
shows that P
ox
, Fe
ox
, and Al
ox
concentrations are useful measures for predict-
ing the P fertilising potential of SOFs in slightly acidic soils.
Multiple linear regression revealed that the OM content may also be a quick and sim-
ple indicator for available P in SOFs as a significant and positive relationship (R
2
= 0.59, p
< 0.01) was found between P-CaCl
2 (pH5.5)
and OM content (Figure 2b). In other words, SOFs
with high OM content released more P-CaCl
2
under acidified conditions. However, there
is no causal relation between the two parameters since the correlation is an effect of the
positive correlation between OM content and P
Fe
(R
2
: 0.78, p < 0.01). As a consequence, the
reliability of OM as an indicator for the easily available P fraction may be limited when
this relation is applied to other SOFs because (i) the relation was derived on a limited
number of samples and (ii) it can be expected that the reliability of OM as an indicator
decreases in samples in which the iron content is strongly influenced by the dosage of iron
salts during the processing process.
Figure 2. The relationships between P-PO
4
(% of Pt) measured in 10 mM CaCl
2
extracts (at initial pH and after acidification
to pH 5.5) and (A) the percentage of P bound to Fe/Al-oxides (P
Fe)
(B) organic matter content (%DW) in the organic ferti-
lisers.
y = 0.03x
R² = 0.02
y = -0.78x + 51.79
R² = 0.71
0
15
30
45
60
75
90
0 10203040506070
P-PO
4
(% of P
t
)
PFe (%)
P-CaCl2
P-CaCl2,pH5.5
Linear (P-CaCl2)
Linear (P-CaCl2,pH5.5)
A
y = 0.09x
R² = 0.31
y = 0.60x - 5.83
R² = 0.59
0
15
30
45
60
75
90
0 102030405060708090100
P-PO
4
(% of P
t
)
OM (% of DW)
B
Figure 2.
The relationships between P-PO
4
(% of Pt) measured in 10 mM CaCl
2
extracts (at initial pH and after acidification
to pH 5.5) and (
A
) the percentage of P bound to Fe/Al-oxides (P
Fe)
(
B
) organic matter content (%DW) in the organic
fertilisers.
Multiple linear regression revealed that the OM content may also be a quick and
simple indicator for available P in SOFs as a significant and positive relationship (R
2
= 0.59,
p< 0.01) was found between P-CaCl
2 (pH5
.
5)
and OM content (Figure 2B). In other words,
SOFs with high OM content released more P-CaCl
2
under acidified conditions. However,
there is no causal relation between the two parameters since the correlation is an effect of
the positive correlation between OM content and P
Fe
(R
2
: 0.78, p< 0.01). As a consequence,
the reliability of OM as an indicator for the easily available P fraction may be limited when
this relation is applied to other SOFs because (i) the relation was derived on a limited
number of samples and (ii) it can be expected that the reliability of OM as an indicator
Agronomy 2021,11, 2233 13 of 18
decreases in samples in which the iron content is strongly influenced by the dosage of iron
salts during the processing process.
3.6. Speciation of P in SOFs and Implications for Their Use in Agriculture
Based on the analytical P pools (Table 4), P
t
in the SOFs was distributed over five
distinct P species as visualised in Figure 3. Easily available P is defined as the fraction
extractable in P-CaCl
2
at pH 5.5. Iron-bound P was calculated using Equations (1)–(3).
Crystalline P is defined as the difference between P
ox
minus P
Fe
and P-CaCl
2,pH5
.
5
. Organic
P is determined with the P
kuo
method. Residual P is defined as the difference between
P
t
determined after wet digestion and P
t,kuo
determined after dry combustion and may
partly exist due to artefacts in the P
t,kuo
method. Hence, the nature and speciation of P in
the residual fraction are unknown.
Agronomy 2021, 11, x FOR PEER REVIEW 14 of 18
Organic P made up a relatively small fraction of P
t
(0.6–21%), which is because part
of the OM has already been mineralised during anaerobic digestion and/composting. The
remaining fraction of organic P may be released over time, depending on the mineralisa-
tion rate of the organic fraction. The rate of this process depends amongst others on the
nature of the OM in the SOF [44] and the mineralisation rates of OM, which are generally
higher for SFs from digestate as compared to composts [47]. Organic matter decomposi-
tion may also influence the release of P bound to Fe/Al oxides by releasing organic acids
which decrease P adsorption onto Fe/Al-oxides due to competition for absorption sites
[19,35,36], though this effect is likely small considering that Fe/Al-oxides in soils are usu-
ally already, to an extent, covered by organic matter [67].
Upon addition of an SOF to soil, P
Fe
present in the SOF might be slowly released over
time due to desorption. The Langmuir equation can be used to describe the concentration
of P-PO
4
in equilibrium with P absorbed to Fe-oxides. The desorption rate is a function of
the difference between the actual P-PO
4
concentration in the soil solution and the equilib-
rium P-PO
4
concentration. Hence, in soils with a low P status, P
Fe
will be slowly released
and be partly reabsorbed onto the mineral surfaces of the receiving soil until a new equi-
librium has been established. In soils with a high P status, meaning a high DPS, Fe-bound
P present in SOFs adds to the total P stock in the soil but does not exert an effect on the P-
PO
4
equilibrium concentration in the soil solution. This implies that the use of SOFs in
which a large fraction of P is bound to Fe/Al oxides at P application rates above crop up-
take, is not likely to increase the risk of P leaching; but will also not increase the labile P
available for plant uptake. Solid organic fertilisers with a large fraction of P bound to Fe/Al
oxides are, therefore, the preferred option for use as organic soil improvers since more
OM can be added to the soil without increasing the risks for P leaching.
Figure 3. Distribution of phosphorus (P) species (% of total P) in solid fractions (SF) of digestate
from different treatment plants, and average P distribution for composted vegetable, fruit and gar-
den waste (VFG-COMP, n:4), composted green waste (GW-COMP, n:2) and sieved soil (Soil, n:3).
The organic fertilisers are put in order of increasing percentage of easily available P.
Figure 3.
Distribution of phosphorus (P) species (% of total P) in solid fractions (SF) of digestate from
different treatment plants, and average P distribution for composted vegetable, fruit and garden
waste (VFG-COMP, n:4), composted green waste (GW-COMP, n:2) and sieved soil (Soil, n:3). The
organic fertilisers are put in order of increasing percentage of easily available P.
The distribution of P
t
between the P species is shown in Figure 3, in which the SOFs
are arranged in order of increasing fraction of easily available P. The SF of digestate from
GZV (GZV-SF1) has by far the highest fraction of easily available P (87% of P
t
) and a
negligible amount of P bound to Fe/Al oxides because the use of Fe salts and Fe-rich
substrates is avoided at this treatment plant. As a result, GZV-SF1 is the preferred fertiliser
if the SOF is supposed to act primarily as a P fertiliser. In the other SFs of digestate, the
percentage of easily available P was lower and this could only partly be explained by
the use of Fe-rich feedstock or Fe-salts and hence binding of P to Fe-oxides. The other
reason for the low availability of P in other SFs is the larger fraction of crystalline P but
it is unknown what causes these differences in the fraction of crystalline P between SFs.
Drying of the SFs of digestates may have led to an increase in the fraction of crystalline P
in SFs of Waterleau New Energy and AmPower. Crystalline P consists of poorly soluble P
precipitates that were insoluble in CaCl
2
at pH 5.5 but dissolved in acid oxalate. Apatite
Agronomy 2021,11, 2233 14 of 18
and struvite are examples of crystalline P precipitates. Struvite is known to dissolve at
pH 5.5 but its dissolution rate is related to the size of the particle and hence, dissolution
of struvite in CaCl
2,pH5
.
5
may not have been complete during the 30-min shaking period.
In acidic soils, the crystalline P fraction is likely slowly released over time whereas this
fraction may remain mostly unavailable for plant uptake when applied to calcareous soils
in which dissolution rates of P precipitates are even lower [17].
In the SF of beet pulp digestate (BP-SF), most of the P was bound to Fe/Al-oxides. At
this plant, Fe sludge was added as an iron source. That sludge is a side product from the
purification of anaerobic groundwater for the production of drinking water and consists
of fine colloidal Fe-hydroxides. Though Fe is added to sorb S
2−
[
66
], the addition of Fe
also exerts a large negative effect on P availability which can be explained by two factors.
First, the binding of P to Fe may result in overdosage of Fe as compared to the amount of
Fe needed to bind H
2
S. Secondly, upon contact with oxygen, sulphides oxidize to form
sulphuric acid and Fe(III)-hydroxides, on which P is sorbed. It is likely that this biologically
mediated process occurs during storage of the SFs. Iron salts or Fe sludge were also used
in AmPower and Waterleau New Energy, yet the percentage of P
Fe
in AMP-SF and WNE-
SF1&2 was small (11–29% of P
t
) compared to P
Fe
in the SF from the beet pulp processing
company (61% of P
t
) which is due to the higher P
t
value and hence lower Fe/P
t
ratio in the
SFs of AmPower and Waterleau New Energy. Nevertheless, avoiding the use of Fe in the
processing of digestate could be a step forward in improving the fertiliser value of SOFs.
An alternative for removing H
2
S from biogas is the use of chemical or biological scrubbers.
Removal of P and enhanced solid-liquid separation can also be fulfilled by adding Mg
salts (MgCl
2
, MgO) forming struvite upon reaction with PO
43−
which is available for plant
uptake. GZV is nowadays using MgCl
2
as an alternative for Fe salts, despite the higher
costs, because they aim to produce a SF that is suitable as a P fertiliser.
In GW composts and sieved soil, P bound to Fe/Al-oxides was the dominant P fraction
which, together with the low OM content of the GW composts (average 27% OM), points
to an abundance of soil mineral particles in GW composts originating from garden waste
including roots and associated soil. Hence, the origin of the Fe in composts differs from that
in SFs of digestate. VFG composts are, in terms of P speciation, in between GW compost
and SFs of digestate with 35% of Ptbeing bound to Fe/Al-oxides.
Organic P made up a relatively small fraction of P
t
(0.6–21%), which is because part of
the OM has already been mineralised during anaerobic digestion and/composting. The
remaining fraction of organic P may be released over time, depending on the mineralisation
rate of the organic fraction. The rate of this process depends amongst others on the nature
of the OM in the SOF [
44
] and the mineralisation rates of OM, which are generally higher
for SFs from digestate as compared to composts [
47
]. Organic matter decomposition may
also influence the release of P bound to Fe/Al oxides by releasing organic acids which
decrease P adsorption onto Fe/Al-oxides due to competition for absorption sites [
19
,
35
,
36
],
though this effect is likely small considering that Fe/Al-oxides in soils are usually already,
to an extent, covered by organic matter [67].
Upon addition of an SOF to soil, P
Fe
present in the SOF might be slowly released over
time due to desorption. The Langmuir equation can be used to describe the concentration of
P-PO
4
in equilibrium with P absorbed to Fe-oxides. The desorption rate is a function of the
difference between the actual P-PO
4
concentration in the soil solution and the equilibrium
P-PO
4
concentration. Hence, in soils with a low P status, P
Fe
will be slowly released and be
partly reabsorbed onto the mineral surfaces of the receiving soil until a new equilibrium
has been established. In soils with a high P status, meaning a high DPS, Fe-bound P present
in SOFs adds to the total P stock in the soil but does not exert an effect on the P-PO
4
equilibrium concentration in the soil solution. This implies that the use of SOFs in which a
large fraction of P is bound to Fe/Al oxides at P application rates above crop uptake, is
not likely to increase the risk of P leaching; but will also not increase the labile P available
for plant uptake. Solid organic fertilisers with a large fraction of P bound to Fe/Al oxides
Agronomy 2021,11, 2233 15 of 18
are, therefore, the preferred option for use as organic soil improvers since more OM can be
added to the soil without increasing the risks for P leaching.
4. Conclusions
Our results provide further evidence that organic fertilisers recovered from digestate
or biowaste are highly variable in terms of their P
t
content and P fertilising potential. Albeit
tedious and time-consuming, the novel method presented here, which is based on CaCl
2
extraction at pH 5.5 and at a fixed total P content, provides a reliable means for assessing P
availability. Easily available P correlated negatively with the fraction of P bound to Fe/Al
oxides (P
Fe
) determined from the oxalate-extractable Fe, Al, and P. As such, P
Fe
could serve
as an indicator for P availability in SOFs. Also, the relationship between easily available P
and P
Fe
revealed that the use of Fe salts or Fe sludge negatively affects the availability of P
in SFs of digestate and should, therefore, be discouraged. Generally, the fraction of easily
available P was higher for SFs of digestate as compared to composted biowaste. When
selecting organic P fertilisers or soil improver, farmers should be made aware of differences
in P speciation among SOFs. SOFs with a high fraction of easily available P, typically SFs
of digestate, are preferably used as P fertilisers to raise the soil P status. Meanwhile, SOFs
with a low fraction of easily available P act as slow-release fertilisers and are, therefore, the
preferred choice in soils prone to P leaching.
Supplementary Materials:
The following are available online at https://www.mdpi.com/article/
10.3390/agronomy11112233/s1, Table S1: Experimental parameters and composition of the CaCl
2
extract solution at the initial pH, Table S2: Experimental parameters and composition of the CaCl
2
extract 30 min after lowering the pH towards 5.0.
Author Contributions:
Conceptualization, I.C.R. and C.E.E.; methodology, I.C.R.; software, C.E.E.;
validation, I.C.R. and C.E.E.; formal analysis, I.C.R. and C.E.E.; investigation, I.C.R. and C.E.E.; re-
sources, I.C.R.; data curation, C.E.E. and I.C.R.; writing—original draft preparation, C.E.E. and I.C.R.;
writing—review and editing, I.C.R., E.M., F.M.G.T. and C.E.E.; visualization, C.E.E.; supervision,
F.M.G.T. and E.M.; project administration, E.M. and F.M.G.T.; funding acquisition, E.M., F.M.G.T. and
I.C.R. All authors have read and agreed to the published version of the manuscript.
Funding:
This research is done as part of the SYSTEMIC project that receives funding from the
European Union’s Horizon 2020 Framework Programme for Research and Innovation under Grant
Agreement no. 730400.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement:
All data generated or analysed during this study are included in the
present article.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.
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