Content uploaded by Yohey Hashimoto
Author content
All content in this area was uploaded by Yohey Hashimoto on Aug 23, 2019
Content may be subject to copyright.
Speciation of Phosphorus Zinc and Copper in Soil and Water-
Dispersible Colloid Affected by a Long-Term Application of Swine
Manure Compost
Kosuke Yamamoto,
†
Yohey Hashimoto,*
,†
Jihoon Kang,
‡
and Kazuki Kobayashi
†
†
Bioapplications and Systems Engineering, Tokyo University of Agriculture and Technology, 2-24-16 Koganei, Tokyo 184-8588,
Japan
‡
School of Earth, Environmental, and Marine Sciences, University of Texas Rio Grande Valley, 1201 West University Drive,
Edinburg, Texas 78539, United States
*
SSupporting Information
ABSTRACT: The objective of this study was to investigate the concentration and chemical
species of Zn, Cu, and P in the bulk soil and water-dispersible colloid (WDC) fraction collected
from a field where swine manure (SM) compost has been continually applied for 23 years. A
filtration and ultracentrifugation process was used to separate and collect WDC (20−1000 nm)
from the soil. The continual application of SM increased soil P from 1.6 to 4.5 g kg−1, Zn from
109 to 224 mg kg−1, and Cu from 87 to 95 mg kg−1for 23 years. The continual SM compost
application also enhanced the formation of soil WDC in which Zn (215 mg kg−1) and Cu (62
mg kg−1) were highly accumulated and P (25 g kg−1) was greater than in the bulk soil. According
to the result of X-ray absorption spectroscopy (XAS), the continual application of SM compost
increased P associated with Fe hydroxides in the soil and WDC fraction. Iron K-edge XAS
revealed the dominance of goethite and ferrihydrite in the WDC fraction, suggesting that P was
bound to these (oxy)hydroxides. Copper K-edge XAS determined the dominance of Cu(II)
associated with humus in the soil and WDC fraction. For Zn species in the SM-compost-applied
soil, hopeite and Zn associated with humus were accumulated in the bulk soil, whereas Zn
associated with humus was the primary species in the WDC fraction. Our study suggests that the formation of organic
complexes in the WDC fraction could enhance the mobility of Zn and Cu as the repeated application of SM compost continues.
■INTRODUCTION
The accumulation of phosphorus (P) and heavy metals of zinc
(Zn) and copper (Cu) is a common issue in soils receiving a
large amount of swine manure (SM) and in farms with pig
production. Among the various types of livestock, SM or pig
slurry contains relatively high levels of Zn and Cu
1
due to the
extensive use of veterinary medicinal products in pig
production.
2
Therefore, the continual application of SM in
the farmland results in the elevation of these elements in soils.
Jensen et al. (2018)
2
reviewed the studies of a long-term field
trial of SM applications and found that the annual loading rate
of Zn increases linearly to the annual accumulation of Zn in
soils with an accumulation rate of 0.96 mg kg−1per year in
Denmark. Another monitoring study on pig-slurry-applied soils
in Denmark reported that 45% of all soil samples collected in
the entire country exceeded the predicted no-effect concen-
trations of Zn for soil organisms.
3
The accumulation of Zn in
soils receiving manure from piglet production farms may be
vulnerable to leaching loss of Zn, particularly in sandy soils.
2
The mobility and potential bioavailability of elements in
soils depend on their oxidation states and chemical species.
According to previous studies using synchrotoron-based X-ray
absorption fine structure (XAFS) spectroscopy, chemical
species of elements have been determined in SM and pig
slurry mainly as struvite
4
for P, hopeite,
4
Zn phosphate,
5
and
ZnS
6
for Zn and Cu associated with organic matter
5
for Cu. It
is largely unknown how the chemical species of elements, in
particular, Zn and Cu in SM, will have been altered in the soil
for a decade or even longer time span. Formentini et al.
(2017)
6
investigated Zn species in the soil to which pig slurry
was continuously applied for 11 years and found that ZnS
abundant in pig slurry was not detected in the soil but had
been transformed and accumulated as Zn associated with
organic matter. A comprehensive study focusing on P, Zn, and
Cu in SM-applied soils is essential because high levels of soil
Zn and Cu detrimentally affect the activity of phosphatases
7
that may affect P species derived from SM in the long term.
Phosphorus, Zn, and Cu in soils interact with each other in
their chemical species, eventually impacting the mobility and
potential availability to biota.
Water-dispersible colloid (WDC) being representative of
readily mobile colloids with a size range of 1−1000 nm plays a
critical role in transport of elements in soils. Previous studies
Received: May 29, 2018
Revised: September 17, 2018
Accepted: October 17, 2018
Published: October 17, 2018
Article
pubs.acs.org/est
Cite This: Environ. Sci. Technol. 2018, 52, 13270−13278
© 2018 American Chemical Society 13270 DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
Downloaded via Yohey Hashimoto on December 20, 2018 at 04:55:52 (UTC).
See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.
observed a drastic increase in Zn, Cu, and P transport in
response to the increase in colloidal transport.
8,9
A notable
accumulation of P and Zn was found in the WDC fraction of
soil and SM compost compared with those bulk samples.
4,10
With the use of synchrotron-based XAFS spectroscopy, these
studies revealed the contrasting differences in chemical species
of P and Zn between bulk soil and WDC phases, suggesting
the relevance of the WDC fraction for elucidating the mobility
and potential bioavailability of elements in soils. Despite the
importance of WDC in the transport and bioavailability of
elements, previous studies have mainly focused on the bulk
soil, particulate, and dissolved fractions (operationally defined
as a <0.45 mm fraction) while neglecting colloidal fractions in
the soil.
The objective of this study was to investigate the
concentration and chemical species of Zn, Cu, and P in the
soil and WDC fraction collected from a field where SM
compost has been continuously applied for 23 years. Long-
term field experiments are essential in revealing the changes in
accumulation and speciation of manure-derived metals and P
in the soil. In Japan, a field experiment was set up in 1993 to
examine the impact of chemical fertilizer (CF) and SM
compost on the accumulation of trace metals, crop
productivity, and soil fertility.
11
Up to the first 10 years, a
rapid increase in Zn, Cu, and P had been observed in the soil
with continual SM compost applications. Studies on the
chemical fractionation of Zn and Cu in the soil demonstrated
the significant increase in oxalate extractable fraction by the
SM application.
12,13
Asada et al. (2012)
12
reported that the
continual application of SM compost was attributed to an
increase in soil water retention and porosity compared with the
soil treated with CF. These results raise the questions how
have Zn, Cu, and P species in CF and SM been transformed in
the soil and WDC fraction and how have these elements, in
particular, in the WDC fraction, have the potential of being
transported out of the field via surface and subsurface
pathways. To address the questions, we used synchrotron-
based XAFS spectroscopy to determine chemical species of Zn,
Cu, and P in the soil and WDC fraction.
■MATERIALS AND METHODS
Soil Characterization. The experimental plots were
located at Western Region Agricultural Research Center,
NARO, Kyoto, Japan and were established in 1993. The plots
had been treated twice a year with CF and SM compost for 23
years. The annual application rate was 360 kg ha−1for CF
(nitrogen basis), 53.2 Mg ha−1for a single dose of SM compost
(SM1), and 159.6 Mg ha−1for a triple dose of SM compost
(SM3, fresh weight basis). The SM compost contained 25 g P
kg−1,701mgZnkg
−1,and257mgCukg
−1(total
concentration). Properties of soil and SM compost and details
of the location and experimental conditions are summarized in
Tables S1 and S2 in the Supporting Information (SI) and
reported elsewhere.
11,12
The soil samples were collected from a
depth of 0−10 cm from the plots to which CF, a single dose of
SM compost (SM1), and a triple dose of SM compost (SM3)
were applied in March 2015. To know the historical changes of
elemental concentration and speciation, we analyzed archived
soil samples collected from these plots between the years 1993
and 2014. Mineral and chemical properties of soils being
collected for 23 years were measured, including soil texture,
pH, elemental concentration, acid ammonium oxalate Fe and
Mn (Feox,Mn
ox), and dithionite−citrate extractable Fe and Mn
(Fed,Mn
d).
Fractionation of Water-Dispersible Colloids. WDCs
from the soils treated with CF and SM compost for 23 years
were fractionated using the procedure of Yamamoto and
Hashimoto (2017)
4
according to the definition of colloid
particle size by IUPAC.
14
In brief, filtration and ultra-
centrifugation processes were employed to collect soil WDC
with particle sizes of 20−1000 nm. The details are shown in
the SI. According to the analysis using dynamic light scattering,
a series of filtration and ultracentrifugation processes enabled
the fractionation of colloidal sized fraction into a filtrate
fraction (≤1000 nm), a WDC fraction (20−1000 nm), and a
dissolved fraction (<20 nm). The WDC fraction was 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 major cations, anions, and total organic
carbon (TOC) were determined in the supernatant of
nonultracentrifuged (≤1000 nm) and ultracentrifuged (<20
nm, dissolved fraction) samples, and the difference between
their concentrations was considered to be associated with
WDCs. The concentration of total P was measured colori-
metrically by potassium−persulfate digestion,
15
followed by
the ascorbic acid and phosphomolybdenum blue method
16
using a UV spectrometer (Shimadzu, Japan). The TOC
concentration was determined by a TOC analyzer (Shimadzu,
Japan). The concentrations of Zn, Cu, and Fe were analyzed
by atomic absorption spectrometry (Z-5010, Hitachi, Japan)
after acid decomposition.
Solution 31P NMR Spectroscopy. Phosphorus extraction
from soil and SM compost following the procedures of
solution 31P NMR analysis was conducted according to the
method described in Turner et al (2003).
17
The methods are
summarized in the SI. Solution 31P NMR spectra were
obtained using JEOL 500 MHz spectrometer (JEOL, Japan).
The NMR parameters were a 45°pulse width, 0.28 s
acquisition time, 1.0 s pulse delay, and up to 21 000 scans at
22 ±1°C. The spectra were processed using JEOL software,
Delta 5.0.1 (JEOL, Japan). The P compounds were identified
by their chemical shifts (ppm). The inorganic ortho-P signal
for each sample was adjusted to 6.0 ppm in all spectra to
simplify the comparisons among samples.
18,19
The spectra
were plotted with 7 Hz line broadening. Signals of NMR
spectra were grouped into P species in accordance with
previous studies.
17,18
Inorganic P compounds included
orthophosphate (6 ppm) and pyrophosphate (−4.3 ppm).
Detected organic P compounds included orthophosphate
monoesters from 6.4 to 7.7 ppm and between 2.9 and 5.7
ppm and orthophosphate diesters from −3.0 to 2.5 ppm.
XAFS Spectroscopy. The XAFS measurements for P, Zn,
Cu, and Fe were conducted for the bulk soil (<2 mm) and
WDC samples. The P K-edge XANES measurements were
conducted at Aichi Synchrotron Radiation Center (Aichi,
Japan) using Beamline BL6N1 equipped with a InSb (111)
monochromator at ambient temperature under a He
atmosphere. References for P compounds and mineral-
adsorbed phases were also analyzed and are summarized in
the SI. The XANES spectra for the samples and reference P
compounds were collected in fluorescent yield mode. The P
concentration was diluted to ∼1% with boron nitride (BN), if
necessary. The monochromator was calibrated at the whiteline
(2481.7 eV) of K2SO4
’s S K-edge XAFS spectrum. The
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13271
background and baseline of all spectra were corrected and
normalized using the Athena software,
20
and linear combina-
tion fitting (LCF) on the XANES spectra of bulk and WDC
samples was performed using all possible binary combinations
of the available P reference compounds. The quality of LCF
results was quantified through a residual (R) value, and the top
three results including the binary and ternary combinations of
references were reported in the SI. The LCF was performed in
the relative energy range between −10 and 30 eV.
The Zn K-edge and Cu K-edge XAFS measurements were
conducted at SPring-8 (Hyogo, Japan) using Beamline
BL01B1 and Aichi Synchrotron Radiation Center (Aichi,
Japan) using Beamlines BL5S1 and BL11S2, both equipped
with a Si(111) monochromator at ambient temperature.
References for Zn and Cu compounds and mineral-adsorption
phases were also analyzed and summarized in the SI.A
reference spectra of Zn associated with kaolinite was provided
by Andreas Voegelin.
21
The Zn K-edge and Cu K-edge XAFS
data were collected in transmission mode for BN-diluted
references and in fluorescent mode with a solid-state detector
or a silicon drift detector for synthesized references and soil
samples at ambient temperature. Energy calibration was made
by the first derivative of the white line peak of Zn foil assigned
at 9659 eV and that of Cu foil assigned at 8979 eV. The XAFS
data were processed using the Athena software (Ravel and
Newville, 2005).
20
To identify which Zn and Cu species were
predominant in the sample, LCF using possible binary and
ternary combinations of Zn and Cu references was performed
on normalized k3-weighted EXAFS spectra between 2.5 and 10
Å−1and on normalized k2-weighted EXAFS spectra between
2.5 and 9.5 Å−1, respectively. The details about the references,
data process, and structural parameters derived from shell-fits
to the EXAFS spectra are given in the SI.
■RESULTS AND DISCUSSION
Characterization of Bulk Soils. The continual application
of SM compost notably increased soil P that was about three
times greater in the soil with a triple dose rate (SM3 soil, 4.5 g
kg−1) than the chemical-fertilizer-applied soil (CF soil, 1.6 g
kg−1) in the 23rd year of field trial (Figure 1a). Compared with
the CF soil, Zn and Cu concentrations in SM3 soil in the 23rd
year of field trial reached 224 and 95 mg kg−1, respectively
(Figure 1b,c). In contrast, the concentrations of these elements
had not virtually changed by the CF application for 23 years.
The continual application of CF decreased the soil pH value
from 6.2 to 4.3 for 23 years, whereas such drastic acidification
of soil was not observed by the continual application of SM
compost (Figure 1d). A notable mineralogical alternation by
23 year SM compost applications was observed in the increase
in poorly crystalline Fe, as indicated by oxalate extractable Fe
(Feox) concentrations (Figure S1), which was attributed to the
addition of ferrihydrite through the application of SM compost
(described later)
Characterization of Water-Dispersible Colloid. Over
99% of WDC collected from the soils was distributed in the
range between 20 and 1000 nm with a mean particle size (Z
average) of 176 ±2 nm for SM1 soil and 205 ±14 nm for
SM3 soil (Figure S2). Because of the small quantity, the size
distribution of WDCs in the CF soil was not determined. The
amount of WDC in the soil increased with increasing SM
application rate. For instance, SM3 soil (2.4 g kg−1) contained
two times greater WDC than SM1 soil (1.2 g kg−1)(Table S3).
A similar amount of WDC was reported in paddy soils (0.8−
2.2 g kg−1, Liang et al.
22
), an upland soil (3.8 g kg−1, Liu et
al.
10
), and SM compost (2.7 g kg−1
4
). The elements consisting
of WDC were mainly Si, Al, and Fe for CF soil, and the
contribution of C to the constituents of WDC increased
notably in the soils treated with continual SM application
(Table S3). Figure 2 illustrates the concentrations of selected
elements in the WDC (20−1000 nm) and dissolved (<20 nm)
fractions, normalized to the mass of the bulk soil. Inorganic P
(Pi), Cu, and Zn were accumulated in the dissolved fraction,
whereas organic P (Po) and Fe were preferentially
concentrated in the WDC fraction. The continual application
of SM compost was attributed to the increase in these elements
in the dissolved and WDC fractions. In SM3 soil, for example,
Pi and Po in the WDC fraction reached 20 and 8.2 mg kg−1,
which were 29 and 41 times greater than those in the CF soil,
respectively. The accumulation of Cu and Zn in the WDC
fraction was pronounced in SM-applied soils, but these
elements were not found in the WDC fraction of CF soil. In
CF soil, Cu and Zn were mostly distributed in the dissolved
fraction (Figure 2).
Phosphorus Species. The solution 31P NMR results
demonstrated that the original soil included P mainly as
inorganic orthophosphate (78%) to a minor extent of organic
P as phosphomonoesters (22%, Figure 3). A continual
application of CF and SM compost (triple dose) until the
year of 2015 increased the proportion of inorganic
orthophosphate in the soil up to 87% (CF2015 and SM2015
soils). The increase in inorganic orthophosphates in SM2015
soil is attributed to the fact that inorganic orthophosphates
occurred mainly in SM compost itself, accounting for 80% of
total P (Figure 3). Compared with SM2015 soil, the
proportion of phosphomonoesters increased to 40% in the
WDC fraction of triple-dose SM-applied soil in 2015
(SM2015WDC). This result suggests that the accumulation
of stable organic phosphates occurs preferentially in the WDC
fraction compared with the bulk soil. Liu et al. (2014)
10
also
reported a similar result demonstrating the enrichment of
phosphomonoesters in the WDC fraction of agricultural soils,
although the bulk soil data were unavailable. The other P
species including pyro- and polyphosphates, phosphodiesters
Figure 1. Concentration of P, Zn, and Cu and pH of soils treated with
chemical fertilizer (CF, open circle) and single and triple doses of
swine manure (SM) compost (filled triangle and square, respectively)
for 23 years.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13272
and phosphonates were nil in the soil, SM, and WDC samples
(Table S4). A very small amount of WDC was operationally
collected from the CF soil in the 2015 sample (CF2015),
probably due to the acidic soil pH (4.3, Table S1) that
decreased the stability and dispersibility of colloids;
23
there-
fore, we were unable to use the WDC for the NMR and the
following XAFS measurements for P as well as Zn and Cu.
All XANES spectra of soil, SM, and WDC samples were
characterized by the pre-edge around 2145 eV (Figure S3),
indicating the presence of PO4associated with Fe minerals.
24
The XANES spectrum of triple-dose SM-compost-applied soil
collected in the year of 2015 (SM2015) was similar to that of
SM compost alone (SM), and these spectra were similar to
those of the hydroxyapatite reference, exhibiting a distinctive
feature at the shoulder on the high-energy side of the white-
line peak.
25,26
These visual observations on the XANES spectra
unambiguously indicate the presence of PO4associated with
Fe and Ca minerals in the samples. Because of the high
similarity in XANES spectra, it is unwise to differentiate PO4
species between adsorbed phases (e.g., P adsorbed on
goethite) and minerals (e.g., strengite). Thus the LCF results
were reported as a group of PO4associates with Fe (Fe−P), Ca
(Ca−P), and Al (Al−P) unless a single PO4species was
predominant in the sample (Figure 4 and Table S5).
Moreover, we used XANES data to determine inorganic
phosphate species in the samples because (i) P K-edge XANES
is not always appropriate for organic P identification in soils
27
and (ii) P in the samples was mainly present as an inorganic
form (Figure 3).
Figure 2. Concentrations of selected elements in the fraction of water-dispersible colloid (20−1000 nm) and dissolved phase (<20 nm) collected
from the soil treated with chemical fertilizer (CF) and single and triple doses of swine manure compost (SM1 and SM3) at the year of 2015. Pi and
Po indicate inorganic and organic P, respectively. A box in panels b and c shows a magnified scale of the yaxis. Note the different scales on the y
axis (panels b and c).
Figure 3. Solution 31P NMR of NaOH-EDTA extract of swine manure (SM) compost and soils treated with chemical fertilizer (CF) and SM
compost and water-dispersible colloid (WDC). Soil1992: the original (untreated) soil collected in 1992; CF2015 and SM2015: soils treated with
chemical fertilizer (CF) and triple-dose SM compost collected in 2015; SM2015WDC: WDC fractionated from SM2015 soil. A magnified x-axis
region is shown in the box. Integration of peak area and the P recovery in the extracts are summarized in the SI.
Figure 4. P K-edge XANES spectra of soil, swine manure (SM), and
water-dispersible colloid (WDC) samples (dots) and their linear
combination fits using P reference spectra (solid lines). Abbreviations
are summarized in the legend of Figure 3.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13273
The concentration of each P species in the soil, WDC, and
SM compost was calculated by multiplying the normalized
proportions of LCF with the total P in each sample (Figure
5a). The original soil (Soil1992) contained 55% Al−P (0.67 g
kg−1) and 39% Fe−P (0.47 g kg−1) as major species. The
continual application of CF for 23 years (CF2015) did not
exhibit a notable change in Al−P concentration but an increase
in the Fe−P concentration from 0.47 to 0.79 g kg−1.In
contrast, the continual application of SM compost for 23 years
(SM2015) rapidly increased the concentration of Fe−P to 3.4
gkg
−1(76%) and Ca−P to 0.86 g kg−1(19%) with a
concomitant decrease in Al−P to 0.23 g kg−1(5%). The
accumulation of these P species in the SM2015 soil
corresponds to the P species in SM that is enriched with
Fe−P (59%) and Ca−P (41%). The accumulation of Fe−P
was more pronounced than that of Ca−P in the soil receiving
SM compost, although these species were present in a similar
proportion in SM compost. A field study reported that during
time of cultivation, there was a progressive shift from Ca−P
and Al−P into Fe−P forms.
28
The increase in Fe−P in soils is
also attributed to higher affinity of P for Fe than Al, which has
been indicated by a model system of mixed ferrihydrite and
boehmite suspensions with <100 mmol PO4kg−1.
29
In
accordance with the result of Fe K-edge XAFS, the Fe mineral
species retaining PO4in the SM2015 soil can be ferrihydrite,
whose proportion to the total Fe has increased from 14 to 34%
in 23-year compost applications (Figure S4, Table S6).
Phosphorus species and their proportions in the WDC
fraction of SM-compost-applied soil (SM2015WDC) were
similar to the SM2015 soil consisting mainly of Fe−P (3.8 g
kg−1, 84%) and a minor extent of Ca−P (0.50 g kg−1, 11%)
and Al−P (0.23 g kg−1, 5%) (Figure 5a). A large proportion of
Fe−P over Al−P in the SM2015WDC corresponds to the high
levels of oxalate extractable Fe (7.0 g kg−1) relative to oxalate
extractable Al (2.6 g kg−1)(Figure S1). The dominance of P
associated with Fe minerals in the soil colloidal fraction has
been reported using XANES spectroscopy,
10
field flow
fractionation methods,
30,31
and an ultrafiltration method.
32
A
soil column study demonstrated that WDC particles enriched
with Fe hydroxides were important carriers for P via the
subsurface water flow.
33
However, none of these studies
identified the specific Fe species that can serve as carriers for P
transport. Our EXAFS study revealed that ferrihydrite and
goethite were the major forms of Fe in the SM2015WDC
sample (Figure S4). These Fe oxyhydroxides usually have <30
nm size;
34
therefore, the accumulation of ferrihydrite and
goethite in the WDC fraction is more pronounced than that of
illite (another form of Fe in WDC, Table S6), which often has
a submicron size distribution.
34
Zinc Species. The overall structure of Zn EXAFS spectrum
for the original soil (Soil1992) and CF-applied soil (CF2015)
is similar to that of Zn associated with kaolinite (Figure 6a).
These soils exhibited a marked splitting in the first oscillation
of their EXAFS spectra at 3.7 Å−1, corresponding to the
reference of Zn associated with kaolinite.
21
The first-shell Zn−
O distance (2.06 Å) and coordination number (5.7 to 5.8)
obtained for Soil1992 and CF2015 corresponded to those of
Zn associated with kaolinite, where Zn is octahedrally
coordinated (Figure S5 and Table S7). Such splitting in the
EXAFS oscillation was less pronounced in the SM-treated soil
(SM2015) and WDC fraction (SM2015WDC), whereas their
overall EXAFS structure was close to the reference spectrum of
Zn associated with humus. The first-shell Zn−O distance (1.99
to 2.01 Å) and coordination number (4.1 to 4.4) for the
SM2015 and SM2015WDC corresponded to those of Zn
associated with humus and hopeite, where Zn is tetrahedrally
coordinated (Figure S5 and Table S7).
On the basis of visual observation and the results of shell fit,
Zn species and their distributions in the soil, WDC, and SM
samples were determined by EXAFS-LCF using the Zn
reference spectra (Figure 6a and Table S8). The concentration
of each Zn species in the samples was calculated by multiplying
the proportions of LCF with the total Zn in each sample
(Figure 5b). The original soil (Soil1992) contained 95% Zn
associated with phyllosilicates (99 mg kg−1) that included
kaolinite and hydroxyl-interlayered montmorillonite (Table
S8). The continual application of CF to the soil (CF2015) did
not virtually change the distribution of these Zn species,
suggesting that Zn-bearing phyllosilicates are stable without
being transformed by soil acidification and mineralogical
alternation from the long-term CF applications (Figure 1 and
Figure S1). In contrast, the continual application of SM
compost for 23 years (SM2015) induced the accumulation of
hopeite (60 mg kg−1, 27%) and Zn associated with humus (72
mg kg−1, 32%) in addition to the inherent species of Zn
associated with phyllosilicate (78 mg kg−1, 35%). This is in
agreement with Zn species in SM compost alone that contains
hopeite (266 mg kg−1, 38%) and Zn associated with humus
Figure 5. Concentrations of P, Zn, and Cu species in the soil, water-
dispersible colloid (WDC), and swine manure (SM) samples
determined by the result of linear combination fit on their XAFS
spectra (panels a−c, respectively). Abbreviations are summarized in
the legend of Figure 3. The category “unknown”in panels b and c is a
group of unknown species of Zn and Cu, in which LCF is unable to
identify a specific species in the sample.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13274
(i.e., analog for Zn associated with organic substances, 205 mg
kg−1, 29%) as primary Zn species (Figure 5b). Thus hopeite
and Zn associated with humus in SM have persisted and
accumulated in the SM2015 soil, giving a notable increase in
soil Zn concentration for 23 years. These Zn species have been
found in a soil with a continual application of pig slurry,
6
in a
sludge-treated soil,
35
and in an elevated P soil.
36
In contrast with the SM2015 soil, a remarkable difference in
Zn species and their proportions was found in the WDC
fraction of soil receiving SM compost (SM2015WDC), where
Zn associated with humus was predominant (79%, 160 mg
kg−1), followed by Zn associated with kaolinite (15%, 30 mg
kg−1). Yamamoto and Hashimoto (2017)
4
reported that Zn
associated with humus was considerably more abundant in the
WDC fraction than in the bulk sample of SM compost. Our
result indicated that hopeite was very minor in the WDC
fraction, although it was a dominant species in SM compost
and the SM2015 soil. Hopeite has been found on a micron-to-
millimeter scale in soil and organic waste.
5,37,38
In our study,
the absence of hopeite and the abundance of Zn associated
with humus in the WDC fraction of SM-applied soil may be
attributed to the difference in their size; therefore, the apparent
size of hopeite precipitates is larger than the range of WDC
fraction (20−1000 nm).
Copper Species. Copper in the bulk soil, WDC, and SM
samples was present as an oxidized form of Cu(II) in
accordance with the position of the white-line peak in the
XANES spectrum (Figure S6). The overall structure of soil Cu
EXAFS spectra was similar to that of Cu associated with
kaolinite (Figure 6b). In the SM-treated soil and WDC sample,
a shoulder at k≈6Å
−1in their EXAFS spectra corresponds to
those of Cu associated with humus.
39
As suggested by previous
studies,
40,41
however, Cu(II)-O coordinating species including
Cu associated with clay minerals and oxides are difficult to be
distinguished by LCF on soil EXAFS spectra due to their
similarity and Jahn−Teller distortion. To narrow down the
number of reference spectra for LCF, we used Cu(II)
associated with kaolinite as an analogous species of Cu
associated with clay minerals and oxides
40
(hereafter Cu-clay)
because kaolinite was identified as a predominant clay mineral.
The concentration of each Cu species in the soil, WDC, and
SM samples was calculated by multiplying the proportions of
LCF with the total Cu in each sample (Figure 5c). The original
soil (Soil1992) contained 95% Cu associated with clay
minerals (Cu-clay, 46 mg kg−1) that was a native Cu species
occurring via pedogenic processes. The continual application
of CF for 23 years (CF2015) indeed induced soil acidification
and mineralogical alternation (e.g., Figure 1) but did not
transform the native Cu species. In contrast, the soil receiving
23 year SM compost (SM2015) showed the accumulation of
Cu associated with humus (41%, 39 mg kg−1) along with Cu
associated with clay minerals (47 mg kg−1) that had persisted
without undergoing transformations. The emergence of Cu
associated with humus in the SM2015 soil was attributed to an
exogenous addition of SM compost containing mainly Cu
associated with humus (172 mg kg−1, 67%) and Cu3(PO4)2
(50 mg kg−1, 19%). Copper species and their proportions in
the WDC fraction of SM-compost-applied soil
(SM2015WDC) were similar to the SM2015 soil consisting
mainly of Cu associated with humus (20 mg kg−1, 44%) and
clay minerals (17 mg kg−1, 38%).
Humic substances in the soil have high affinity for Cu.
39,41,42
Copper in the SM2015 and SM2015WDC samples was
accumulated as organically associated forms, suggesting that it
Figure 6. Spectra of Zn K-edge EXAFS (a) and Cu K-edge EXAFS (b) of selected references, soil, water-dispersible colloid (WDC), and swine
manure (SM) samples (circles) and their linear combination fits using reference spectra (solid lines). Abbreviations are summarized in the legend
of Figure 3. The best results of LCF are shown on the right side of each panel. The sum of components of LCF on each sample is not adjusted to
100%. Zn phyllo: the sum of Zn associated with kaolinite and montmorillonite. Cu-clay: the sum of Cu associated with kaolinite and gibbsite.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13275
is a chemically stable species in the soil without trans-
formations via physicochemical interactions. It has been
reported that humic acid enhances the adsorption of Cu(II)
on phyllosilicates
43
and hematite.
44
Such a mechanism of
Cu(II) binding to humus is associated with the formation of
ternary complexes with Fe(III) in goethite, where a bridging
metal is centered between Cu and organic functional groups.
45
Cu(II) also forms ternary complexes binding both organic
substances and Al,
46,47
enabling them to be stable and
accumulated in soils, although such a mechanism was not
confirmed in this study. It should be noted that copper
phosphate [Cu3(PO4)2] was a secondary Cu species in SM
compost but was not found in the soil receiving SM compost
(Figure 5c). To the best of our knowledge, none of studies has
identified Cu associated with PO4in P-enriched soils.
48
Copper phosphate compounds in SM compost may be
responsible for the transformations into more stable forms,
some of which were probably Cu associated with humus in this
study (Figure 5c).
Environmental Implication. Agricultural soils receiving a
large amount of SM and located on farms with swine
production can be a primary source of Zn and Cu in the
environment. With the application rate in SM compost used in
this study, the total input of Zn and Cu for the 23 year field
trial was estimated to be 0.91 and 0.33 Mg ha−1(on a dry
weight basis and 1.0 g mL−1soil bulk density), and we
expected their concentrations to reach approximately 916 and
335 mg kg−1in the top 10 cm of soil, respectively. Considering
the actual concentration of Zn and Cu in the 23rd year of field
trial, it was assumed that about 71 and 76% of Zn and Cu
added through SM compost had been lost from the top 10 cm
of soil, plausibly by plant uptake and surface and subsurface
transport pathways. Because the plant uptake of these
micronutrients is small or even negligible relative to their
input from SM compost, the excess Zn and Cu would be
mainly lost with soil particles (i.e., WDC) via surface runoff
and leaching to the subsurface. A loss of Zn and Cu from the
field may be explained by the very coarse texture of soil (>60%
sand) that can contribute to percolation of solute containing
Zn and Cu as dissolved and WDC phases. Ogiyama et al.,
2005
1
found that Zn and Cu derived from pig manure leached
readily in a sandy soil compared with fine texture soils. Prior to
our study, Asada et al. (2012)
12
investigated soil physical
properties in the 13th year of the field trial and found that the
continual SM application increased soil hydraulic conductivity
(wet conditions) to two orders of magnitude greater than the
continual CF application. Along with the remarkable increase
in soil Zn and Cu levels in the current study, the continual
application of SM compost to soils for 23 consecutive years
likely gradually altered the soil physical properties to more
favorable conditions for Zn and Cu transport via WDC.
In soils receiving repeated land applications of SM and pig
slurry, the concentration and speciation changes of Zn, P, and
Cu over time are critical in predicting the long-term fate and
potential mobility of these elements. Our study suggests that a
continual application of SM compost to soils significantly
increases the concentration of Zn and Cu, and these metals
accumulate as organically complexed forms in the bulk soil and
WDC fraction. The enrichment of organically associated Zn
and Cu in the WDC fraction indicates the elevated leaching
potential of these metals. Previous studies demonstrated that
WDC in soils and biosolid enhanced Zn and Cu transport in a
laboratory soil column experiment.
9,49
Mineralization and
disaggregation of organic matter associated with Zn and Cu
may trigger the release of these metals to the dissolved
phase.
5,50
In addition to Zn and Cu, our study demonstrated
that the continual SM compost application increased P
associated with Fe minerals in the soil and WDC fraction
(Figure 5a). In a soil condition enriched with organic matter,
phosphate binding to Fe(III) is prone to be associated with
humic substances (i.e., ternary complexes),
8,30,51
resulting in an
enhanced transportation of P in manure-applied soils.
52
The
transport of animal waste-derived P was found to be facilitated
by the competition between P and dissolved organic carbon for
anion adsorption sites,
53
implying the significance in P bound
to WDC and ternary P complexes for the elucidating
environmental fate of P. Our study suggests that the long-
term land application of SM should monitor the accumulation
and speciation of heavy metals (Zn and Cu) and nutrient
elements (P) over time to minimize the environmental loss of
these elements.
■ASSOCIATED CONTENT
*
SSupporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.est.8b02823.
Table S1. Characterization of soil before (year 1992)
and after treated with CF and single and triple doses of
SM compost for 23 years. Table S2 Characterization of
CF and SM compost. Figure S1. Oxalate extractable Fe
and Al in the soils treated with CF and single and triple
doses of SM compost for 23 years. Figure S2. Particle
size distribution in solution collected from the soils
treated with a single and triple dose of SM at the year of
2015, determined by a dynamic light scattering method.
Table S3. Concentrations of WDC and elements in
WDC collected from the soils treated with CF and single
and triple doses of SM compost in the year of 2015.
Table S4. Concentration of relative percentage of
functional inorganic and organic P groups in NaOH-
EDTA extracts of soils and SM compost by solution 31P
NMR. Table S5. The best result and second- and third-
best results of binary and ternary combinations of LCF
on P K-edge XANES spectra of samples. Figure S3. P K-
edge XANES spectra of samples, AlPO4and FePO4·
2H2O in a pre-edge region from 2143 to 2148 eV. Figure
S4. First-derivative of Fe XANES spectra and EXAFS
spectra of samples and their results of linear combination
fitting using Fe reference compounds. Table S6. The
best result and second- and third-best results of binary
and ternary combinations of LCF on Fe K-edge EXAFS
spectra of samples. Table S7. Structural characterization
of Zn in the reference compounds and samples by shell
fitting in R-space of EXAFS spectra using theoretical
paths. Table S8. The best result and second- and third-
best results of binary and ternary combinations of LCF
on Zn K-edge EXAFS spectra of samples. Figure S5.
Experimental and fitting data for Fourier-transformed
EXAFS spectra for selected Zn reference compounds
and soil, SM, and WDC samples. Table S9. The best
result and second- and third-best results of binary and
ternary combinations of LCF on Cu K-edge EXAFS
spectra of samples. Figure S6. Cu K-edge XANES
spectra of reference compounds and samples. Table S10.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13276
Copper reference compounds used for Cu K-edge XAFS
measurements. (PDF)
■AUTHOR INFORMATION
Corresponding Author
*E-mail: yhashim@cc.tuat.ac.jp.
ORCID
Yohey Hashimoto: 0000-0002-0321-929X
Notes
The authors declare no competing financial interest.
■ACKNOWLEDGMENTS
We are grateful to Erika Sato and Ayako Fukunaga (National
Agriculture and Food Research Organization) for providing
archived soil samples and for their support for the field work.
We thank Andreas Voegelin (Swiss Federal Institute of Aquatic
Science and Technology) for kindly providing a XAFS
reference spectrum. The XAFS spectroscopy experiments
were conducted using Beamline BL01B1 at SPring-8, Japan
Synchrotron Radiation Research Institute, Hyogo, Japan
(proposal numbers: 2016B1565 and 2016B1181) and Beam-
line BL5S, BL6N1, and BL11S2 at Aichi Synchrotron
Radiation Center, Aichi Science & Technology Foundation,
Aichi, Japan. This study was funded in part by KAKENHI
Grant-in-Aid for Scientific Research (B) 15H04467, provided
from the Ministry of Education, Culture, Sports, Science, and
Technology, Japan.
■REFERENCES
(1) Ogiyama, S.; Sakamoto, K.; Suzuki, H.; Ushio, S.; Anzai, T.;
Inubushi, K. Accumulation of Zinc and Copper in an Arable Field
after Animal Manure Application. Soil Sci. Plant Nutr. 2005,51, 801−
808.
(2) Jensen, J.; Kyvsgaard, N. C.; Battisti, A.; Baptiste, K. E.
Environmental and public health related risk of veterinary zinc in pig
production - Using Denmark as an example. Environ. Int. 2018,114,
181−190.
(3) Jensen, J.; Larsen, M. M.; Bak, J. National monitoring study in
Denmark finds increased and critical levels of copper and zinc in
arable soils fertilized with pig slurry. Environ. Pollut. 2016,214, 334−
340.
(4) Yamamoto, K.; Hashimoto, Y. Chemical Species of Phosphorus
and Zinc in Water-Dispersible Colloids from Swine Manure Compost.
Journal of Environmental Quality 2017,46, 461−465.
(5) Tella, M.; Bravin, M. N.; Thurie
s, L.; Cazevieille, P.; Chevassus-
Rosset, C.; Collin, B.; Chaurand, P.; Legros, S.; Doelsch, E. Increased
zinc and copper availability in organic waste amended soil potentially
involving distinct release mechanisms. Environ. Pollut. 2016,212,
299−306.
(6) Formentini, T. A.; Legros, S.; Fernandes, C. V. S.; Pinheiro, A.;
Le Bars, M.; Levard, C.; Mallmann, F. J. K.; da Veiga, M.; Doelsch, E.
Radical change of Zn speciation in pig slurry amended soil: Key role
of nano-sized sulfide particles. Environ. Pollut. 2017,222, 495−503.
(7) Kunito, T.; Saeki, K.; Goto, S.; Hayashi, H.; Oyaizu, H.;
Matsumoto, S. Copper and zinc fractions affecting microorganisms in
long-term sludge-amended soils. Bioresour. Technol. 2001,79, 135−
146.
(8) Hens, M.; Merckx, R. Functional Characterization of Colloidal
Phosphorus Species in the Soil Solution of Sandy Soils. Environ. Sci.
Technol. 2001,35, 493−500.
(9) Karathanasis, A. D. Subsurface migration of copper and zinc
mediated by soil colloids. Soil Sci. Soc. Am. J. 1999,63, 830−838.
(10) Liu, J.; Yang, J.; Liang, X.; Zhao, Y.; Cade-Menun, B. J.; Hu, Y.
Molecular Speciation of Phosphorus Present in Readily Dispersible
Colloids from Agricultural Soils. Soil Sci. Soc. Am. J. 2014,78,47−53.
(11) Hori, K.; Fukunaga, A.; Ojima, K.; Suga, Y.; Urashima, Y.;
Tanaka, K.; Ikeda, J. The behavior of zinc in vegetable cropping fields
using cattle or pig feces compost. Bull. Natl. Agric. Res. Cent. West. Reg.
2005,4, 109−128.
(12) Asada, K.; Yabushita, Y.; Saito, H.; Nishimura, T. Effect of long-
term swine-manure application on soil hydraulic properties and heavy
metal behaviour. European Journal of Soil Science 2012,63, 368−376.
(13) Ito, A.; Murayama, S.; Ikeda, J.; Fukunaga, A.; Hori, K.
Chemical forms and dilute hydrochloric acid extractability of
potassium, manganese, iron, copper and zinc in soils of vegetable
cropping field using for long term cattle or pig feces compost. Jpn. J.
Soil Sci. Plant Nutr. 2010,81, 563−572.
(14) Slomkowski, S.; Aleman, J. V.; Gilbert, R. G.; Hess, M.; Horie,
K.; Jones, R. G.; Kubisa, P.; Meisel, I.; Mormann, W.; Penczek, S.;
Stepto, R. F. T. Terminology of polymers and polymerization
processes in dispersed systems (IUPAC Recommendations 2011).
Pure Appl. Chem. 2011,83, 2229−2259.
(15) Martin, M.; Celi, L.; Barberis, E. Determination of low
concentrations of organic phosphorus in soil solution. Commun. Soil
Sci. Plant Anal. 1999,30, 1909−1917.
(16) Murphy, J.; Riley, J. P. A modified single solution method for
the determination of phosphate in natural waters. Anal. Chim. Acta
1962,27,31−36.
(17) Turner, B. L.; Mahieu, N.; Condron, L. M. Phosphorus-31
nuclear magnetic resonance spectral assignments of phosphorus
compounds in soil NaOH-EDTA extracts. Soil Sci. Soc. Am. J. 2003,
67, 497−510.
(18) Hill, J. E.; Cade-Menun, B. J. Phosphorus-31 nuclear magnetic
resonance spectroscopy transect study of poultry operations on the
Delmarva Peninsula. J. Environ. Qual. 2009,38, 130−138.
(19) Hashimoto, Y.; Watanabe, Y. Combined applications of
chemical fractionation, solution 31P-NMR and P K-edge XANES to
determine phosphorus speciation in soils formed on serpentine
landscapes. Geoderma 2014,230−231, 143−150.
(20) Ravel, B.; Newville, M. Athena, artemis, hephaestus: data
analysis for X-ray absorption spectroscopy using IFEFFIT. J.
Synchrotron Radiat. 2005,12, 537−541.
(21) Jacquat, O.; Voegelin, A.; Kretzschmar, R. Local coordination
of Zn in hydroxy-interlayered minerals and implications for Zn
retention in soils. Geochim. Cosmochim. Acta 2009,73, 348−363.
(22) Liang, X.; Jin, Y.; Zhao, Y.; Wang, Z.; Yin, R.; Tian, G. Release
and migration of colloidal phosphorus from a typical agricultural field
under long-term phosphorus fertilization in southeastern China. J.
Soils Sediments 2016,16, 842−853.
(23) Seta, A. K.; Karathanasis, A. D. Stability and Transportability of
Water-Dispersible Soil Colloids. Soil Science Society of America Journal
1997,61, 604−611.
(24) Hesterberg, D.; Zhou, W. Q.; Hutchison, K. J.; Beauchemin, S.;
Sayers, D. E. XAFS study of adsorbed and mineral forms of
phosphate. J. Synchrotron Radiat. 1999,6, 636−638.
(25) Hashimoto, Y.; Takamoto, A.; Kikkawa, R.; Murakami, K.;
Yamaguchi, N. Formations of Hydroxyapatite and Inositol Hexaki-
sphosphate in Poultry Litter during the Composting Period:
Sequential Fractionation, P K-edge XANES and Solution 31P NMR
Investigations. Environ. Sci. Technol. 2014,48, 5486−5492.
(26) Maguire, R. O.; Hesterberg, D.; Gernat, A.; Anderson, K.;
Wineland, M.; Grimes, J. Liming Poultry Manures to Decrease
Soluble Phosphorus and Suppress the Bacteria Population. J. Environ.
Qual. 2006,35, 849−857.
(27) Hesterberg, D. Macroscale Chemical Properties and X-ray
Absorption Spectroscopy of Soil Phosphorus. In Synchrotron-Based
Techniques in Soils and Sediments; Singh, B., Grafe, M., Eds.; Elsevier:
Oxford, U.K., 2010; pp 313−356.
(28) Nurwalera, J. Soil Phosphorus Dynamics during Continuous
Cultivation in a Brazilian Amazon Oxisol. M.Sc. Thesis, North
Carolina State University, Raleigh, NC, 1991.
(29) Khare, N.; Hesterberg, D.; Beauchemin, S.; Wang, S.-L. XANES
determination of adsorbed phosphate distribution between ferrihy-
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13277
drite and boehmite in mixtures. Soil Sci. Soc. Am. J. 2004,68, 460−
469.
(30) Regelink, I. C.; Koopmans, G. F.; van der Salm, C.; Weng, L.;
van Riemsdijk, W. H. Characterization of Colloidal Phosphorus
Species in Drainage Waters from a Clay Soil Using Asymmetric Flow
Field-Flow Fractionation. Journal of Environmental Quality 2013,42,
464−473.
(31) Henderson, R.; Kabengi, N.; Mantripragada, N.; Cabrera, M.;
Hassan, S.; Thompson, A. Anoxia-Induced Release of Colloid- and
Nanoparticle-Bound Phosphorus in Grassland Soils. Environ. Sci.
Technol. 2012,46, 11727−11734.
(32) Turner, B. L.; Kay, M. A.; Westermann, D. T. Colloidal
Phosphorus in Surface Runoff and Water Extracts from Semiarid Soils
of the Western United States. J. Environ. Qual. 2004,33, 1464−1472.
(33) Makris, K. C.; Grove, J. H.; Matocha, C. J. Colloid-mediated
vertical phosphorus transport in a waste-amended soil. Geoderma
2006,136, 174−183.
(34) Bigham, J. M.; Fitzpatrick, R. W.; Schulze, D. G. Iron Oxides. In
Soil Mineralogy with Environmental Applications; Amonette, J. E.,
Bleam, W. F., Schulze, D. G., Dixon, J. B., Eds.; Soil Science Society of
America: Madison, WI, 2002; pp 323−366.
(35) Kirpichtchikova, T. A.; Manceau, A.; Spadini, L.; Panfili, F.;
Marcus, M. A.; Jacquet, T. Speciation and solubility of heavy metals in
contaminated soil using X-ray microfluorescence, EXAFS spectrosco-
py, chemical extraction, and thermodynamic modeling. Geochim.
Cosmochim. Acta 2006,70, 2163−2190.
(36) Panfili, F. R.; Manceau, A.; Sarret, G.; Spadini, L.;
Kirpichtchikova, T.; Bert, V.; Laboudigue, A.; Marcus, M. A.;
Ahamdach, N.; Libert, M. F. The effect of phytostabilization on Zn
speciation in a dredged contaminated sediment using scanning
electron microscopy, X-ray fluorescence, EXAFS spectroscopy, and
principal components analysis. Geochim. Cosmochim. Acta 2005,69,
2265−2284.
(37) Sarret, G.; Balesdent, J.; Bouziri, L.; Garnier, J.-M.; Marcus, M.
A.; Geoffroy, N.; Panfili, F.; Manceau, A. Zn Speciation in the Organic
Horizon of a Contaminated Soil by Micro-X-ray Fluorescence, Micro-
and Powder-EXAFS Spectroscopy, and Isotopic Dilution. Environ. Sci.
Technol. 2004,38, 2792−2801.
(38) Donner, E.; Howard, D. L.; Jonge, M. D. D.; Paterson, D.;
Cheah, M. H.; Naidu, R.; Lombi, E. X-ray Absorption and Micro X-
ray Fluorescence Spectroscopy Investigation of Copper and Zinc
Speciation in Biosolids. Environ. Sci. Technol. 2011,45, 7249−7257.
(39) Strawn, D. G.; Baker, L. L. Molecular characterization of copper
in soils using X-ray absorption spectroscopy. Environ. Pollut. 2009,
157, 2813−2821.
(40) Fulda, B.; Voegelin, A.; Ehlert, K.; Kretzschmar, R. Redox
transformation, solid phase speciation and solution dynamics of
copper during soil reduction and reoxidation as affected by sulfate
availability. Geochim. Cosmochim. Acta 2013,123, 385−402.
(41) Manceau, A.; Matynia, A. The nature of Cu bonding to natural
organic matter. Geochim. Cosmochim. Acta 2010,74, 2556−2580.
(42) Karlsson, T.; Persson, P.; Skyllberg, U. Complexation of
Copper(II) in Organic Soils and in Dissolved Organic Matter −
EXAFS Evidence for Chelate Ring Structures. Environ. Sci. Technol.
2006,40, 2623−2628.
(43) Arias, M.; Barral, M. T.; Mejuto, J. C. Enhancement of copper
and cadmium adsorption on kaolin by the presence of humic acids.
Chemosphere 2002,48, 1081−1088.
(44) Komy, Z. R.; Shaker, A. M.; Heggy, S. E. M.; El-Sayed, M. E. A.
Kinetic study for copper adsorption onto soil minerals in the absence
and presence of humic acid. Chemosphere 2014,99, 117−124.
(45) Alcacio, T. E.; Hesterberg, D.; Chou, J. W.; Martin, J. D.;
Beauchemin, S.; Sayers, D. E. Molecular scale characteristics of Cu(II)
bonding in goethite-humate complexes. Geochim. Cosmochim. Acta
2001,65, 1355−1366.
(46) Fitts, J. P.; Persson, P.; Brown, G. E.; Parks, G. A. Structure and
Bonding of Cu(II)−Glutamate Complexes at the γ-Al2O3−Water
Interface. J. Colloid Interface Sci. 1999,220, 133−147.
(47) Enid Martínez, C.; Martínez-Villegas, N. Copper−Alumina−
Organic Matter Mixed Systems: Alumina Transformation and Copper
Speciation As Revealed by EPR Spectroscopy. Environ. Sci. Technol.
2008,42, 4422−4427.
(48) Mamindy-Pajany, Y.; Sayen, S.; Mosselmans, J. F. W.; Guillon,
E. Copper, Nickel and Zinc Speciation in a Biosolid-Amended Soil:
pH Adsorption Edge, μ-XRF and μ-XANES Investigations. Environ.
Sci. Technol. 2014,48, 7237−7244.
(49) Karathanasis, A. D.; Johnson, D. M. C.; Matocha, C. J. Biosolid
Colloid-Mediated Transport of Copper, Zinc, and Lead in Waste-
Amended Soils Technical article no. 04−06−159. J. Environ. Qual.
2005,34, 1153−1164.
(50) Parat, C.; Denaix, L.; Le
veque, J.; Chaussod, R.; Andreux, F.
The organic carbon derived from sewage sludge as a key parameter
determining the fate of trace metals. Chemosphere 2007,69, 636−643.
(51) Gerke, J.; Hermann, R. Adsorption of orthophosphate to
humic-Fe-complexes and to amorphous Fe-oxide. Z. Pflanzenernaehr.
Bodenkd. 1992,155, 233−236.
(52) Tarkalson, D. D.; Leytem, A. B. Phosphorus Mobility in Soil
Columns Treated With Dairy Manures and Commercial Fertilizer.
Soil Sci. 2009,174,73−80.
(53) Kang, J.; Amoozegar, A.; Hesterberg, D.; Osmond, D. L.
Phosphorus leaching in a sandy soil as affected by organic and
inorganic fertilizer sources. Geoderma 2011,161, 194−201.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.8b02823
Environ. Sci. Technol. 2018, 52, 13270−13278
13278
