Published March 17, 2017
Journal of Environmental Quality
Short Communications
Chemical Species of Phosphorus and Zinc in Water-Dispersible
Colloids from Swine Manure Compost
Kosuke Yamamoto and Yohey Hashimoto*
A
ccumulation of phosphorus (P) and zinc (Zn)
Abstract
is a concern in agricultural soils where intensive and
long-term applications of swine manure are practiced
(Martinez and Peu, 2000; Penha et al., 2015). The effluence of
P and Zn from swine manure and from soil applied with swine
manure can be accelerated by colloidal particles (1–1000 nm
in accordance to the International Union of Pure and Applied
Chemistry definition) (Slomkowski et al., 2011). Hens and
Merckx (2001) reported that P associated with colloidal particles accounts for approximately 75% of effluent P from agricultural soils. Karathanasis (1999) reported that Zn mobility in
soils increased 5- to 50-fold in the presence of colloidal particles.
Regarding the effects of colloidal particles on bioavailability of
elements, Montalvo et al. (2015) demonstrated that colloidal
particles increased P bioavailability in a study on P uptake flux by
wheat, which accelerated five times in the presence of colloidal
P than with dissolved P only. Despite the importance of colloidal fractions in transport and bioavailability, studies have mainly
focused on P in particulate and dissolved fractions (operationally
defined as a <0.45-mm fraction) and thereby have neglected colloidal fractions in environmental samples.
Water-dispersible colloids (WDCs) are representative of
readily mobile colloids because of the high dispersibility and
mobility in the soil solution (de Jonge et al., 2004). Phosphorus
concentrations in WDC fractions (5.31 g kg-1) can be significantly greater than in bulk soil (0.90 g kg-1) (Liu et al., 2013,
2014). In addition to the concentration differences, chemical species of elements in WDCs are critical for understanding
mobility and bioavailability. The use of X-ray absorption fine
structure (XAFS) spectroscopy provides detailed and precise
information on P and Zn species in the soils and WDCs. To the
best of our knowledge, there are few XAFS-based studies determining P and Zn species in the WDCs in environmental samples. Recently, Liu et al. (2014) determined hydroxyapatite and
P associated with iron (Fe) in WDCs collected from agricultural
soils. In a column experiment using a polluted soil, X-ray absorption near-edge structure (XANES) investigations revealed that
the majority of Zn in WDCs was associated with montmorillonite (Lin et al., 2015).
The release of phosphorus (P) and zinc (Zn) from swine manure
compost and from soils applied with swine manure compost
can be accelerated by colloidal particles. This study investigated
the concentrations and chemical species of P and Zn in waterdispersible colloids (WDCs) collected from swine manure
compost by using X-ray absorption fine structure (XAFS)
spectroscopy. A filtration and ultracentrifugation process was
used to separate and collect WDCs (20–1000 nm) from the bulk
swine manure compost (<2 mm). The swine manure compost
contained 2.7 g kg-1 WDC, in which P (140 g kg-1) was highly
concentrated and Zn concentrations were greater than in the
bulk compost (1.45 g kg-1). Phosphorus K-edge X-ray absorption
near-edge structure (XANES) spectroscopy determined the
presence of struvite (NH4MgPO4·6H2O) as a major P species (74%),
followed by tricalcium phosphate as a secondary component
(26%). In the WDC fraction, struvite was not found, but tricalcium
phosphate (56%) occurred as a primary component. Zinc
K-edge XAFS spectroscopy determined hopeite [Zn3(PO4)2·4H2O,
59%] and to a lesser extent smithsonite (ZnCO3, 24%) and Zn
adsorbed on ferrihydrite (17%). In the WDC fraction, hopeite
(44%) and organically bound Zn (35%) were predominant. Our
results demonstrate the notable difference in the concentration
and chemical species of P and Zn between the WDC and bulk
fractions of swine manure compost.
Core Ideas
• We investigated chemical species of P and Zn in the WDC collected from swine manure compost.
• Struvite was not found in WDC, but tricalcium phosphate and P
adsorbed on ferrihydrite were predominant.
• Hopeite and organically bound Zn were predominant in the
WDC fraction.
Copyright © American Society of Agronomy, Crop Science Society of America, and
Soil Science Society of America. 5585 Guilford Rd., Madison, WI 53711 USA.
All rights reserved.
J. Environ. Qual. 46:461–465 (2017)
doi:10.2134/jeq2016.11.0433
This is an open access article distributed under the terms of the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Supplemental material is available online for this article.
Received 8 Nov. 2016.
Accepted 17 Jan. 2017.
*Corresponding author ([email protected]).
Tokyo Univ. of Agriculture and Technology, 2-24-16 Koganei, Tokyo 184-8588,
Japan. Assigned to Associate Editor Markus Gräfe.
Abbreviations: EXAFS, extended X-ray absorption fine structure; LCF, linear
combination fitting; TOC, total organic carbon; WDC, water-dispersible colloid;
XAFS, X-ray absorption fine structure; XANES, X-ray absorption near-edge
structure.
461
The objective of this study was to investigate the concentration and chemical species of P and Zn in WDCs collected from
swine manure compost. Information of chemical species of P and
Zn in bulk and WDC phases of swine manure compost is essential to elucidate how they undergo transformations in the soil via
chemical and biological processes. The WDCs were fractionated
from swine manure compost by aqueous dispersion followed
by ultracentrifugation; P and Zn species in WDCs were determined using synchrotron-based XAFS spectroscopy.
Materials and Methods
Fractionation of Water-Dispersible Colloids
Water-dispersible colloids from a swine manure compost
sample were fractionated using the procedure of Liu et al.
(2014), with a slight modification using a 1-mm filter instead
of a 1.2-mm filter (Ilg et al., 2005) according to the definition
of colloid particle size by the International Union of Pure and
Applied Chemistry (Slomkowski et al., 2011). Triplicates of
6.0-g, air-dried compost samples were passed through a 2-mm
sieve and weighed into 250-mL centrifuge bottles and shaken
with 180 mL of deionized water for 1 h. The suspensions were
then centrifuged (700 × g, 5 min) (20PR-5, RPR12–2, Hitachi
Corp.), and the supernatants were filtered through filter paper
(no. 101, ADVANTEC) to remove coarse particles. The filtrates
were then passed through a 1000-nm microporous membrane.
Approximately 70-mL aliquots of the filtrates were ultracentrifuged (220,000 × g, 20 h) (Optima MAX-XP, MLA-50,
Beckman Coulter, Inc.) to collect WDCs consisting of particles that were 20 to 1000 nm in accordance with Stokes’ law
(Gimbert et al., 2005). According to the analysis using dynamic
light scattering, the series of filtration and ultracentrifugation
processes enabled the fractionation of a colloidal-sized fraction
into a filtrate fraction (≤1000 nm), a WDC fraction (20–1000
nm), and a dissolved fraction (<20 nm) (Supplemental Fig.
S1). The WDCs were freeze-dried after being frozen initially
at -80°C, and the dried mass was subsequently obtained. The
supernatant separated from the filtrate was considered to be a
dissolved fraction.
Concentrations of P, Mg, Ca, Fe, Zn, and total organic carbon
(TOC) were determined in the supernatant of nonultracentrifuged (<1000 nm) and ultracentrifuged (<20 nm) samples,
and the difference between their concentrations was considered
to be associated with WDCs (Ilg et al., 2005). The concentration of P was measured colorimetrically by potassium-persulfate
digestion (Martin et al., 1999) followed by the ascorbic acid and
phosphomolybdenum blue method (Murphy and Riley, 1962)
using an ultraviolet spectrometer (Shimadzu Corp.). The TOC
concentration was determined by a TOC analyzer (Shimadzu
Corp.). The concentrations of Mg, Ca, Fe, and Zn were analyzed
by atomic absorption photometer (Z-5010, Hitachi Corp.) after
acid decomposition.
Phosphorus K-Edge XANES Spectroscopy
The P K-edge XANES spectra for bulk (<2 mm) and WDCs
of swine manure compost were obtained at Aichi Synchrotron
Radiation Center (Aichi, Japan) using a Beamline BL6N1
equipped with a InSb(111) monochromator at ambient temperature under a He atmosphere. References for P compounds
462
were also analyzed, including strengite (FePO4·2H2O), variscite
(AlPO4·2H2O), tricalcium phosphate [Ca3(PO4)2], hydroxyapatite [Ca5(PO4)3OH], struvite (MgNH4PO4·6H2O), phytic acid
sodium salt hydrate (C6H18O24P6· xNa·yH2O), and P adsorbed
on ferrihydrite, goethite, and gibbsite. The XANES spectra for
the compost samples and reference P compounds were collected
in fluorescent yield mode. The P concentration was adjusted to
~1% with boron nitride if necessary. The monochromator was
calibrated at the whiteline (2481.7 eV) of K2SO4’s S K-edge
XAFS spectrum. The background and baseline of all spectra
were corrected and normalized using Athena software (Ravel
and Newville, 2005), and linear combination fitting (LCF) on
the XANES spectra of bulk and WDC samples was performed
using all possible binary combinations of the available P reference compounds, including the ones identified in the samples
by XRD (Hashimoto et al., 2014). The quality of LCF results
was quantified through a residual value, and the top three results
are reported in the supplemental information. The LCF was performed in the relative energy range between -10 and 30 eV. A
detailed description of the methods for the data process is provided in the supplemental information.
Zinc K-Edge XAFS Spectroscopy
The Zn K-edge XAFS spectra for the bulk and WDCs of
swine manure compost were obtained at SPring-8 (Hyogo, Japan)
using Beamline BL01B1 and at the Aichi Synchrotron Radiation
Center (Aichi, Japan) using Beamline BL5S1 equipped with a
Si(111) monochromator at ambient temperature. References for
zinc compounds were also analyzed, including zincite (ZnO),
smithsonite (ZnCO3), zinc hydroxide [Zn(OH)2], zinc acetate
[Zn(CH3COO)2, analog for Zn associated with organic substances], zinc nitrate [Zn(NO3)2], hopeite [Zn3(PO4)2·4H2O],
sphalerite (ZnS), zinkosite (ZnSO4), and Zn adsorbed on ferrihydrite, goethite, gibbsite, birnessite, kaolinite, and montmorillonite. The Zn K-edge XAFS data were collected in transmission
mode for boron nitride–diluted references and in fluorescent
mode with a 19-element Ge semiconductor detector for synthesized references and compost samples at ambient temperature.
Energy calibration was made by the white line peak of ZnO
assigned at 9660 eV. The XAFS data were processed using Athena
software (Ravel and Newville, 2005). To identify which Zn species were predominant in the sample, LCF using possible binary
and ternary combinations of Zn references was performed on
normalized k3–weighted extended X-ray absorption fine structure (EXAFS) spectra between 2.5 and 10 Å-1. The LCF was
also performed on the normalized XANES spectra of samples.
The details of the Zn references and data process are provided in
the supplemental information.
Results and Discussion
Characterization of Water-Dispersible Colloids
The swine manure compost contained 2.7 ± 0.3 g kg-1
WDCs. Bao et al. (2011) reported a similar mass of WDCs in
swine manure (2.8 g kg-1). Liu et al. (2014) found 3.8 to 5.8 g
kg-1 WDCs in rice and vegetable-cultivated soils. These and
our results suggest that the WDCs may be accumulating in soils
rather than in swine manure. The greater amount of WDCs collected from the soil than from manure could be associated with
Journal of Environmental Quality
the particle density of WDC particles such as clays and oxide
minerals, which have greater density than organic materials and
tend to be more abundant in soils than in manure. Because the
compost was made entirely from swine manure (i.e., with little
bedding material), high levels of P were concentrated in the bulk
compost (159 g kg-1) and in the WDCs (140 g kg-1) collected
from the compost (Table 1; Supplemental Table S1). Zinc accumulated in the bulk compost (1.45 g kg-1) and WDCs (2.20 g
kg-1). Bao et al. (2011) reported that the WDCs (0.02–1.00
mm) collected from swine manure contained 422 g TOC kg-1,
18.7 g Ca kg-1, and 3.1 g Fe kg-1, but the concentrations of P
and Zn were not reported. Compared with the result by Bao et
al. (2011), the WDCs collected in this study had greater TOC
and Fe concentrations and a smaller Ca concentration. As compared to the WDCs from swine manure (Bao et al., 2011) and
from swine manure compost (this study), the WDCs collected
from different cultivated soils (Liu et al., 2014) accumulated less
organic C (9.5–24.6 g TOC kg-1) and P (1.2–5.2 g kg-1) and
more or equal amounts of Fe (21.5–19.0 g kg-1) and Ca (8.6–
11.0 g kg-1).
result indicates that struvite is a major P component (74%) in the
bulk sample, followed by tricalcium phosphate as a secondary
component (26%). The abundance of struvite in the bulk compost is in agreement with XRD results (Supplemental Fig. S2).
Ajiboye et al. (2007) used LCF of P K-edge XANES and found
that swine manure contained variscite (18%), phytic acid calcium (C6H6Ca6O24P6, 32%), and calcium phosphate dihydrate
(CaHPO4·2H2O, 50%). According to their research, struvite
was identified in beef cattle manure (68%) and poultry manure
(12%) but not in swine manure. Organic P was scarce relative
to inorganic P because solution 31P nuclear magnetic resonance
spectroscopy determined that (i) 99% of P in the bulk compost
was present as inorganic forms and (ii) there were trace amounts
(<1%) of P mono- and diesters and no phytic acid (i.e., myo-inositol hexakisphosphate; Supplemental Fig. S3).
In contrast to the bulk compost, struvite was not found in the
WDCs, but tricalcium phosphate (56%) was the primary component, as evidenced by the best- and second-best results of LCF
(Fig. 1b; Supplemental Table S5). The LCF determined that P
adsorbed on ferrihydrite (44%) was a secondary species in the
WDCs. The second-best result of LCF determined P adsorbed
on gibbsite (33%) as a secondary P species in the WDCs, suggesting that P associated with Fe and Al hydroxide minerals accumulates in the WDCs of swine manure compost. The absence of
struvite and the abundance of calcium phosphate in the WDCs
may be attributed to their size of crystals, or more practically
their aggregate size of individual crystallites. The size of crystals
forming in an aqueous solution is much smaller for hydroxyapatite (<1 mm) than struvite (18–50 mm) (Hutnik et al., 2011). The
Phosphorus K-Edge XANES Spectroscopy
Figure 1 shows P K-edge XANES spectra of bulk compost
and WDC samples together with P reference compounds that
yielded the best fits by LCF analysis. The difference between
XANES spectra from bulk compost and WDCs was characterized by the shoulder between 2150 and 2155 eV and a small
peak at 2159 eV. The overall curvature of P-XANES spectrum
for the bulk compost is similar with that for struvite. The LCF
Table 1. Characterization of bulk sample and water-dispersive colloid (WDC) of swine manure compost†.
Fraction
Bulk (<2 mm)
WDC (20–1000 nm)
Total organic C
P
Mg
Ca
Fe
Zn
———————————————————————————— g kg−1 ————————————————————————————
235 ± 2‡
159 ± 4
23.3 ± 0.2
64.9 ± 0.9
5.1 ± 0.1
1.45 ± 0.02
739 ± 41
140 ± 31
9.1 ± 1.3
12.9 ± 0.8
5.6 ± 0.4
2.2 ± 0.5
† The methods and additional data for characterization of bulk compost were shown in supporting information.
‡ Values are means ± SD.
Fig. 1. Phosphorus K-edge X-ray absorption near-edge structure spectra for (a) bulk compost and (b) water-dispersible colloids (WDCs) and their
best results of binary linear combination fitting with reference spectra.
Journal of Environmental Quality463
greater aggregate size of struvite is in large part a reflection of the
considerably greater hydration energy of Mg than Ca in tricalcium phosphate, resulting in the exclusion of struvite from the
WDC fraction.
Zinc K-Edge EXAFS Spectroscopy
The overall structure of Zn EXAFS spectrum for the bulk
compost and WDCs was similar to that of hopeite. Linear combination fitting on the Zn EXAFS spectrum of bulk compost
indicated that hopeite was the primary species, accounting for
59% of total Zn (Fig. 2). The predominance of hopeite in the
bulk compost was also supported by the second-best result of
EXAFS-LCF (Supplemental Table S6) and by the best result
of XANES-LCF (60%) (Supplemental Fig. S5; Supplemental
Table S7). Smithsonite (24%) and Zn adsorbed on ferrihydrite
(17%) were identified as secondary components, with a similar
abundance in the bulk compost. Smithsonite has been directly
identified in alkaline soil systems (Mattigod et al., 1986), suggesting that a part of Zn was stabilized as a form of smithsonite in the alkaline bulk compost (pH 9.2) (Supplemental Table
S1). These results correspond overall to a previous study (Tella
et al., 2016), reporting the presence of Zn-phosphate and Zn
associated with ferrihydrite in manure compost from pig slurry.
The majority of P in the compost sample occurred in inorganic
forms (Supplemental Fig. S3), indicating that Zn was bound
mainly with inorganic P (i.e., hopeite) and that the occurrence
of Zn associated with organic P (e.g., Zn phytate) was unlikely.
Meanwhile, Legros et al. (2010) reported that Zn bound to
organic matter was the most predominant species in pig slurry,
according to the result of EXAFS-LCF using a reference of Zn
acetate.
Similar to the bulk sample, hopeite (44%) was identified in
the WDC fraction as the primary Zn species. The presence of
hopeite in WDCs was also confirmed by the second-best result
of EXAFS-LCF (Supplemental Table S6) and the best result
of XANES-LCF (50%) (Supplemental Fig. S5; Supplemental
Table S7). Smithsonite and Zn adsorbed on ferrihydrite were
not found in WDCs, but Zn acetate (analog for organically
bound Zn, 35%) was identified as a secondary component. The
notable increase of organically bound Zn in WDCs relative to
the bulk compost corresponded to the enrichment of organic
carbon (739 g kg-1) in WDCs (Table 1). It should be noted that
Zn acetate is not as ideal as a surrogate spectrum for organically
bound Zn, and further Zn K-edge XAFS data are needed to
improve the LCF result and our understanding of Zn complexation in the organic matter fractions of bulk compost and WDC
particles. The LCF analysis on the WDC sample revealed a low
concentration of Zn nitrate (21%), which can be representative
of Zn bound weakly to the solid surface (i.e., outer-sphere surface
complex) or Zn in the water-soluble fraction. This is in agreement with the observation that about 12% (153 mg kg-1) of Zn
in the compost sample was water extractable, and some of the
water-soluble Zn could have remained in residual water during
the freeze-drying process of WDCs after aqueous dispersion.
Conclusions
We determined molecular speciation of P and Zn in WDCs
collected from swine manure compost using XAFS spectroscopy.
464
Fig. 2. Zinc K-edge extended X-ray absorption fine structure spectra
(k3–weighted) of reference compounds, bulk compost, and water-dispersible colloids (WDCs) (dotted black lines), their linear combination
fitting using the reference spectra (solid gray lines), and residuals
(dashed gray lines). Hopeite, Zn3(PO4)2·4H2O; smithsonite, ZnCO3,
Zn-ferrihydrite, Zn adsorbed on ferrihydrite.
The forms of P and Zn were different between the bulk compost and WDCs, demonstrating that the precipitate forms of
P (struvite, solubility product constant, Ksp, = 10-13.1) and Zn
(hopeite, Ksp = 10-35.2) were predominant in the bulk compost,
whereas accumulation of P adsorbed on ferrihydrite and organically bound Zn was notable in WDCs. Our study suggests that
P in the WDC fraction may be more stable and less mineralizable than in bulk compost, whereas organically bound Zn in
WDCs is potentially bioavailable and/or repartitions onto other
soil minerals as the organic matter fraction degrades. Our study
Journal of Environmental Quality
also demonstrates the significance of direct determination of P
and Zn species in the WDC fraction relative to the bulk sample,
which improves the assessment of their long-term fate and transport in soil and aquatic systems. Further studies are needed to
determine the chemical species of nutritional and toxic elements
in WDCs in relation to their bioavailability and transport.
Acknowledgments
The authors thank Noriko Yamaguchi (National Agriculture and Food
Research Organization, Tsukuba, Japan) for providing some Zn XAFS
spectra, Hiroshi Oji (Aichi Synchrotron Radiation Center, Japan) for
support for the XAFS experiment, Koki Toyota (Tokyo University of
Agriculture and Technology, Japan) for providing the compost sample,
and Markus Gräfe (Associate Editor of JEQ) for a critical review of a
version of the manuscript. The XAFS spectroscopy experiments were
conducted using Beamline BL01B1 at SPring-8, Japan Synchrotron
Radiation Research Institute, Hyogo, Japan (proposal numbers:
2011B1218 and 2015A1667), and Beamline BL5S and BL6N1 at
Aichi Synchrotron Radiation Center, Aichi Science & Technology
Foundation, Aichi, Japan (proposal numbers: 201503080, 2016P3001,
201603012, 201603013, and 201604101). This study was funded in
part by KAKENHI Grant-in-Aid for Scientific Research (B) 15H04467
and Grant-in-Aid for Scientific Research (C) 15KT0116, provided from
the Ministry of Education, Culture, Sports, Science, and Technology,
Japan. Supporting information is available for characterization of
swine manure compost, particle size distribution of WDCs, XRD,
and solution 31P-NMR of bulk compost as well as the methods of data
process and results of LCF for P and Zn XAFS spectroscopy.
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