Speciation, bioavailability and preservation of phosphorus in surface

sediments of the Changjiang Estuary and adjacent East China Sea

inner shelf
Jia Meng
a, b
, Peng Yao
a, c, d,
*
, Zhigang Yu
a, d
, Thomas S. Bianchi
e
, Bin Zhao
a, b
,
Huihui Pan
a, b
, Dong Li
a, b
a
Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Qingdao 266100, China
b
College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, China
c
Qingdao Collaborative Innovation Center of Marine Science and Technology, Qingdao 266100, China
d
Institute of Marine Organic Geochemistry, Ocean University of China, Qingdao 266100, China
e
Department of Geological Sciences, University of Florida, Gainesville, FL 32611-2120, USA
a r t i c l e i n f o
Article history:
Received 8 November 2013
Accepted 20 April 2014
Available online 29 April 2014
Keywords:
phosphorous
biogeochemical cycle
chemical speciation
bioavailability
preservation
sediments
a b s t r a c t
The speciation, potential bioavailability and preservation of phosphorus (P) in surface sediments of the
Changjiang (Yangtze River) Estuary and adjacent East China Sea (ECS) inner shelf were investigated
through the analyses of P fractions and sediment bulk properties. A sequential extraction method
(SEDEX) was used to separate and quantify the following six sedimentary P reservoirs: exchangeable P
(ExeP), authigenic P (AueP), detrital P (DeeP), organic P (OreP), refractory P (ReeP) and Fe-bound P (Fe
eP). Total P (TP) in surface sediments ranged from 15.0 to 21.4 mmol g
1
and was highest near the
Changjiang river mouth. The average contribution of each form of P to TP was 55.6% (DeeP), 17.8% (ReeP),
16.1% (OreP), 5.5% (AueP), 2.5% (ExeP) and 2.5% (FeeP), respectively. DeeP showed relatively higher
concentrations in the river mouth and the ECS shelf region, off the Changjiang Estuary. High concen-
trations of OreP were found mainly in mud areas showing a similar distribution pattern with silt,
sediment surface area (SSA), and total organic carbon (TOC). ReeP was mainly distributed near the
estuarine area and the ZheeMin coast. Bioavailable P (BAP), accounted for 9.5e32.0% of TP (with a mean
of 21.2%) and showed a similar distribution pattern to that of OreP. DeeP/SSA and TOC/SSA loadings both
decreased with increasing of SSA, while OreP/SSA loadings varied little with SSA, indicating that OreP
may have reached an adsorptionedesorption equilibrium on mineral surfaces. TOC to total organic P
(TOP; sum of ReeP and OreP) ratios less than the Redeld ratio (84 in average) may have indicated
efcient remineralization of organic matter in mobile muds of the Changjiang Estuary and adjacent ECS
inner shelf. Furthermore, the relatively high TOC/OreP ratios (72e422 with a mean of 188) likely suggest
a higher degree of preferential regeneration of labile OreP over TOC in sediments.
2014 Elsevier Ltd. All rights reserved.
1. Introduction
Phosphorus (P) is an essential nutrient and plays a key role in
biogeochemical cycles of biogenic elements in estuarine and
coastal environments (Slomp, 2011), especially for large-river
delta-front estuaries (LDE) (Bianchi and Allison, 2009). The sour-
ces of P in these environments mainly include particulate inor-
ganic/organic materials derived from riverine inputs, marine
autotrophic production and atmospheric dusts (Slomp, 2011, and
references therein). Past work has shown that burial of P in marine
sediments is an important sink and that the fate of P in sediments is
largely controlled by the reactivity of different forms of P (e.g.
Ruttenberg, 1992; Andrieux-Loyer and Aminot, 1997; Coelho et al.,
2004; Hou et al., 2009). Refractory P phases, such as detrital apatite
(Detrital P, DeeP) and other P-containing minerals (derived mainly
from rivers) have slow formation kinetics, are buried directly and
are slow to regenerate (Ruttenberg, 1992; Anschutz et al., 1998;
Coelho et al., 2004). Signicant partitioning and transformation of
reactive P phases occur during burial processes driven by a number
of biological, physical, and geochemical processes (Schenau and de
Lange, 2001; Fang et al., 2007). The interactions of these complex
biogeochemical processes will affect the retention and ultimate
* Corresponding author. Institute of Marine Organic Geochemistry, Ocean Uni-
versity of China, Qingdao 266100, China.
E-mail addresses: yaopeng@ouc.edu.cn, pengyours@gmail.com (P. Yao).
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science
j ournal homepage: www. el sevi er. com/ l ocat e/ ecss
http://dx.doi.org/10.1016/j.ecss.2014.04.015
0272-7714/ 2014 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science 144 (2014) 27e38
form of buried P (Ruttenberg, 1992; Andrieux-Loyer and Aminot,
1997). For example, microbial breakdown of labile sedimentary
organic matter (SOM) results in the release of phosphate, together
with dissolved organic phosphorus (DOP), nitrate, methane and
carbon dioxide, to the overlying water column where it is available
for primary production (Andrieux-Loyer and Aminot, 1997). These
linkages with marine primary productivity and sediment biogeo-
chemical cycling, in part highlight the importance of studying the
speciation and preservation of P in marine sediments (Andrieux-
Loyer and Aminot, 1997; Schenau and de Lange, 2001; Fang et al.,
2007; Hou et al., 2009).
Rapid development of the local economy in the Changjiang
River drainage basin has changed land-use practices which has
partly resulted in large increases in nutrient inputs to the Chang-
jiang LDE. Moreover, P has been shown to be a limiting nutrient for
phytoplankton growth in the Changjiang LDE and the East China
Sea (ECS) shelf (Liu et al., 2003). Thus, any increase in the release of
P from surface sediments to overlying waters could have a signi-
cant impact on phytoplankton production and community
composition. As mentioned earlier, this release from sediments is
largely governed by the speciation of P in sediments (Ruttenberg,
1992; Coelho et al., 2004). Previous work on P cycling in sedi-
ments of the Changjiang LDE and adjacent shelf have mainly
focused on the distribution of P forms and their relationships with
grain size composition (Rao and Berner, 1997; He et al., 2009a) and
bioavailability of particulate P (He et al., 2009b; Hou et al., 2009),
with very few on the preservation of P (Fang et al., 2007). In
addition, previous results either focused on the Changjiang Estuary
(intertidal at) (Xu et al., 2001; Hou et al., 2009) or fromfurther off-
shore (middle shelf) (Zheng et al., 2003; Fang et al., 2007) in the
ECS, with very fewon the outer estuary and inner shelf regions (He
et al., 2009b). More specically, studies on the unique roles of mud
deposits in determining the source and fate of different forms of P
in the highly-reactive mud regions of the Changjiang LDE (Liu et al.,
2007) and/or the ECS inner shelf, have been largely ignored.
This study examined the sources, distributionpatterns, potential
bioavailability and preservation of different forms of P, and their
effects on the Changjiang LDE and the ECS inner shelf, with
particular emphasis on the mobile-mud belts. The primary goal of
this work was to better constrain the biogeochemical processes in P
cycling in the Changjiang LDE, by determining how several sedi-
ment bulk parameters, such as grain size and mineral compositions,
total organic carbon (TOC), and sediment surface area (SSA) inter-
acted with P speciation.
2. Materials and methods
2.1. Study area and sample collection
The Changjiang River is the largest river in China, ranked third in
length (6300 km), fth in freshwater discharge (9.0 10
11
m
3
yr
1
),
and fourth in sediment discharge (4.8 10
8
t yr
1
) in the world
(Dagg et al., 2004). The Changjiang LDE is characterized by high
productivity that largely stems from the high amounts of nutrients
discharged by the river (Zhou et al., 2008). An increase in the
loading of nutrients has also caused severe eutrophication in the
Changjiang LDE, resulting in the frequent occurrence of harmful
algal blooms and seasonal hypoxia in bottom waters (Zhou et al.,
2008). However, recent work has suggested that these eco-
environmental issues were caused mainly by an imbalance in the
nutrient structure, rather than simply high nutrient loadings (Jiang
et al., 2010).
The hydrographic regimes of the Changjiang LDE and the ECS
inner shelf are very complex and are mainly controlled by the
Yellow Sea Coastal Current (YSCC) in the north, the ZheeMin
Coastal Current (ZMCC), and the Taiwan Warm Current (TWWC) in
the south e as well as the Changjiang Diluted Water (CJDW) (Fig. 1)
(Liu et al., 2007). All of the aforementioned currents play a key role
in the transport and burial of sediments from the Changjiang.
Previous investigations have shown that about 40% of the sedi-
ments are deposited in the near-shore just off the river mouth,
forming the Changjiang LDE mud area with high sedimentation
rates ranging from 1 to 6 cmyr
1
(Guo et al., 2003; Liu et al., 2007).
Much of the remaining sediment is transported southward along
the ZheeMin coast by the CJDW and littoral currents (YSCC and
ZMCC), where it is deposited west of 123

E due to a barrier and/or

shear effect of the northward owing TWWC, forming the mobile-
mud belt on the ECS inner shelf (Fig. 1) (Qin et al., 1996; Liu et al.,
2007). Only a small portion of this sediment escapes to the
northeast of the estuary in summer due to enhanced northeast-
ward ow of the CJDW and TWWC (Liu et al., 2006b).
Sampling was conducted onboard the R/V Runjiang 1 (Zhoushan
Runhe Co., Ltd., China) fromlate July to early August in 2011 (Fig. 1).
Surface sediment samples (approx. 5 cm) were collected using a
stainless-steel box-corer in the Changjiang LDE and the ECS inner
shelf. Sediment cores were extruded, cut into sections homoge-
nized, and stored at 20

C until analysis. Most of the samples were

collected within the Changjiang LDE and ZheeMin coastal mud
areas.
2.2. Analyses of sediment grain size, surface area and mineral
composition
Grain size composition of the samples was measured using a
laser particle size analyzer (Mastersizer 2000, Malven Instruments
Ltd., UK), following the method of Hu et al. (2009). Sediment sur-
face area (SSA) was determined using an automatic nitrogen
Fig. 1. Sampling locations at the Changjiang (Yangtze River) Estuary and adjacent East
China Sea (ECS) inner shelf. Arrows indicate the direction of the currents (from Liu
et al., 2007). YSCC: Yellow Sea Coastal Current; TWWC: Taiwan Warm Current;
YSMW: Yellow Sea Mixing Water; ZMCC: ZheeMin Coastal Current; CJDW: Changjiang
Diluted Water. The mud deposits (in shade of orange) are displayed according to Qin
et al. (1996). (For interpretation of the references to color in this gure legend, the
reader is referred to the web version of this article.)
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 28
adsorption surface area analyzer (3H-2000BET-A, Beishide
Instrument-ST Co., Ltd., China), according to Waterson and Canuel
(2008).
The bulk mineralogical composition of the surface sediments
was determined using a Bruker D8 Advance X-Ray. Diffractometer
(XRD) equipped with a copper anode (40 kV, 40 mA) after grinding
and homogenization of samples to < 150 mm. The diffractograms
were collected for each sample over 2q values ranging from 3

to
100

at a step size of 0.02

, and a 1 s counting time per step. Relative

contents of illilite, chlorite, kaolinite, quartz and feldspar were
quantied by the Rietveld method (Young, 1993).
2.3. Organic carbon analysis
Approximately 1 g of freeze-dried sediment was homogenized
and pulverized, and then treated with 6 M HCl to remove inorganic
carbon (mainly in the form of carbonate). Sediments were subse-
quently rinsed with Milli-Qwater to remove salts (Xing et al., 2011).
Inorganic carbon-free samples were then dried in an oven at 60

C
prior to instrumental analysis. Approx. 20 mg of each sample was
carefully crimp-sealed in the tin capsules and analyzed in duplicate
on a Thermo Flash 2000 elemental analyzer. Replicate analysis of
well-mixed samples gave a precision of 0.02 wt. % for TOC (n 6).
2.4. Sequential extraction and analysis of phosphorus
Speciation of P in freeze-dried and homogenized sediment (ca.
0.1 g) was determined by a modied sequential extraction proce-
dure (SEDEX) (Vink et al., 1997). Briey, the method consists of six
steps separating the major reservoirs of sedimentary P into the
following six pools: exchangeable P (ExeP); organic P (OreP); Fe-
bound P (FeeP); authigenic P (AueP); detrital P (DeeP); and re-
fractory P (ReeP) using 1 M MgCl
2
, sodium dodecyl sulfate solution
(SDS), citrate-dithionite-bicarbonate (CDB), acetate buffer, 1 M
HCl(before ashing under 550

C), and 1 M HCl(for ashed residue)
(Ruttenberg, 1992; Vink et al., 1997). More specically, each fraction
is dened as follows: ExeP is formed by direct adsorption of
phosphate onto sediments, FeeP is P associated with oxide or
oxyhydroxide of iron and manganese, AueP included authigenic
carbonate uorapatite (CFAP), biogenic apatite (i.e., bones, teeth,
etc.), and carbonate-associated P (Hou et al., 2009; Sekula-Wood
et al., 2012), Dee P was dened as the P intrinsic to igneous or
metamorphic rocks (Ruttenberg, 1992), OreP contained ortho-
phosphate monoesters (e.g., inositol phosphates) and diesters
(DNA, phospholipids), as well as polyphosphates and pyrophos-
phates that are inorganic storage compounds and degradation
products (Lukkari et al., 2009), and ReeP was dened as organic P
that could not be extracted by SDS. Compared with the original
SEDEX method, this modied method included an additional step
when extracting OreP by SDS. This allowed for separation of OreP
from ReeP (Vink et al., 1997), which is a critical improvement,
because of the difculty of ReeP utilization and that OreP can be
easily regenerated, making the calculation of bioavailable P (BAP)
possible (Lpez-Gutirrez et al., 2004). All extracted phosphates
were determined directly using the spectrophotometric phospho-
molybdate blue method (Murphy and Riley, 1962). Total P (TP)
concentration was the sum of these six particulate P forms. Method
blanks and standard reference materials (SRMs) were used for data
quality control. Sediments standards of China off-shore (GB W
07314) were used as SRMs. The TP concentration for the standard
materials of off-shore marine sediments from China Seas (GBW
07314), was found to be 20.73 1.63 mmol g
1
(relative standard
deviation (RSD) < 10%, n 6), very close to the established value of
this sediment standard (20.85 1.97 mmol g
1
). The RSD of repli-
cate analyses of a given sample were less than 4.5%, 6.9%, 8.7%,
13.0%, 5.9% and 9.9% for ExeP, OreP, FeeP, AueP, DeeP and ReeP,
respectively (n 6).
2.5. Statistical analysis
Pearson correlation analysis, with a two-tailed test of signi-
cance, was performed using the IBM SPSS Statistics 20 program to
study the relationship between the measured parameters. This
program was also used to run one-way ANOVA to determine
whether the spatial variations of P species were statistically sig-
nicant at the 95% condence level.
3. Results
3.1. Bulk properties of surface sediments in the Changjiang Estuary
and adjacent shelf
Surface sediments in the study area were primarily composed of
silt (4e63 mm), which accounted for 25.7%e77.5% (64.9% in
average) of total sediments (Table S1). The median grain size ranged
from 5.8 to 100.8 mm with a mean of 19.1 mm. Fine-grained sedi-
ments were found predominantly in the Changjiang LDE and Zhee
Min coastal mud areas, while coarser sandy sediments mostly
occurred near the Changjiang river mouth (site #9), and the outer
shelf region off the mud area (site #20 and 30)(Table S1). SSA of
surface sediments ranged from 3.49 to 19.96 m
2
g
1
with an
average of 14.77 m
2
g
1
, with the high SSA sediments found mainly
in the Changjiang LDE and ZheeMin coastal mud deposits
(Table S1).
The TOC contents in the surface sediments varied from 0.21 to
0.85% with an average of 0.57% (Table 1). Lower TOC contents were
mainly found near the river mouth and on the outer shelf off the
estuary, where sand contents were high. Conversely, high TOC
sediments were found in the mud areas, characterized by high silt
contents and high SSA (Table 1 and S1).
The mineral composition of surface sediments in this study was
mainly composed by illite, chlorite, kaolinite, quartz and feldspar
(Table 1). Illite was the most abundant mineral in the sediments,
accounting for 4.0e62.7% of the total minerals with an average of
33.7%. Chlorite, quartz and feldspar ranked after illite in abundance,
representing 5.5e39.1%, 6.4e38.5% and 5.7e30.4% of the total
minerals, respectively; fractions of kaolinite was relatively small.
Large size minerals (quartz and feldspar) were mainly distributed
near the river mouth and the near-shore area of the ZheeMin coast.
Small size minerals (illite, chlorite and kaolinite) were mainly
found in the Changjiang LDE mud area and the off-shore region of
the ZheeMin coast, which mostly but not entirely followed the
distributions of sediment grain size and SSA.
3.2. Phosphorus fractions in surface sediments
The concentrations of TP in surface sediments ranged from 15.0
to 21.4 mmol g
1
with an average of 17.0 mmol g
1
, with the highest
TP concentration observed near the river mouth (Table 2). The
distribution of TP outside the Changjiang LDE and ZheeMin coast
was homogeneous, but showed a general decreasing trend moving
seaward (Fig. 2). The DeeP concentrations ranged from 6.60 to
13.2 mmol g
1
with a mean of 9.45 mmol g
1
(Table 2). Similar to
sandy sediments, higher concentrations of DeeP were mainly
found near the river mouth and on the outer shelf region off the
Changjiang LDE, whereas lower values were observed in the mud
areas (Fig. 2c). Concentrations of OreP and ReeP were 0.82e
4.27 mmol g
1
(average in 2.73 mmol g
1
) and 1.72e3.93 mmol g
1
(average in 3.03 mmol g
1
), respectively. OreP showed a similar
distribution pattern with silt, SSA and TOC with high values found
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 29
in the mud areas, while ReeP was mainly distributed throughout
the outer region off the Changjiang LDE and ZheeMin coast
(Fig. 2d). The concentrations of AueP, ExeP and FeeP were rela-
tively low, about an order of magnitude lower than those of other P
forms mentioned above (Table 2).
4. Discussion
4.1. Phosphorus speciation in surface sediments
In general, DeeP concentrations in this study were lower than
those from intertidal sediments of the Changjiang LDE (Hou et al.,
2009) and middle shelf of the ECS (Fang et al., 2007), but were
higher than other estuaries and marginal seas, such as the Arabian
Sea (Schenau and de Lange, 2001), Amazon River and estuary
(Berner and Rao, 1994), Gulf of Mexico (Ruttenberg and Berner,
1993), Mississippi River (Sutula et al., 2004) (Fig. 3). DeeP
accounted for 55.6% of TP (40.6e73.9%), which was very close to the
values from the intertidal sediments of the Changjiang LDE (54.9%)
(Hou et al., 2009), and surface sediments of the Changjiang LDE and
adjacent areas (51.2%) (He et al., 2009b). However, our DeeP was
lower than those found in the middle shelf of the ECS (70.4%) by
Fang et al. (2007) and the Changjiang river mouth (64%) (Rao and
Berner, 1997). These differences were likely due to higher con-
tents of coarser sediments in these two marine settings (Table S1).
In fact, the sediments from sites #9 and #20 were characterized by
sandy sediments, and the fractions of DeeP in TP reached 61.9% and
73.9%, respectively (Table 3). Similarly, the DeeP fractions found in
the Changjiang LDE were higher than other estuaries and marginal
seas around the world at the similar TP levels (Table 3). For
example, DeeP accounted for only about 6% of TP in the Amazon
Estuary (Berner and Rao, 1994) and less than 30% in the Amazon
continental shelf (Rao and Berner, 1997; Ruttenberg and Goi,
1997). Conversely, the Yellow River Estuary, the Bohai Sea, and
the Yellow Sea of China were all characterized by high DeeP con-
tributions(Liu et al., 2004), similar to the Changjiang LDE. One
possible explanation for these differences is that eroded soils from
the upper basins of the Changjiang and Yellow Rivers transported
by the rivers to the Eastern Marginal Seas of China are enriched in
DeeP, whereas rivers like the Amazon, which mainly ows through
tropical rain forests, tropical grasslands and alpine plant regions
(with fertile soils), have a more limited DeeP contribution (Berner
and Rao, 1994; Liu et al., 2006a). This concept is supported by the
high concentrations and percentages of DeeP in suspended par-
ticulate matters (SPM) of the YellowRiver and the Changjiang River
(He et al., 2009a). In addition, we found positive correlations be-
tween DeeP and sand (r 0.61, p < 0.01, n 20), quartz (r 0.56,
p < 0.01, n 20), and inverse relationships between DeeP and clay
(r 0.68, p <0.001, n 20), TOC (r 0.85, p <0.001, n 20) and
SSA (r 0.78, p < 0.001, n 20) (Fig. 4a, b, c). These correlations
can be attributed to the fact that DeeP is mainly composed by
primary minerals, such as quartz and feldspar, which are the major
components of coarse silt, sand and other sediments that have a
large particle size, small-SSA and low-TOC (Keil et al., 1997). Quartz
and feldspar are relatively low in ne-grained TOC-rich sediments,
and thus DeeP concentrations are very low in these sediments.
Recent work on P speciation of size-fractionated surface sediments
in the Changjiang LDE and adjacent areas (using a water elutriation
method (He et al., 2009b)), showed that larger hydrodynamic sizes
(32e63 mm and >63 mm) were also associated with higher con-
centrations and percentages of DeeP.
Table 1
Total organic carbon (TOC) and mineral composition in surface sediments from the Changjiang Estuary and adjacent ECS inner shelf.
Sampling site Latitude (

N) Longitude (

E) TOC (%) Illilite (%) Chlorite (%) Kaolinite (%) Quartz (%) Feldspar (%) Small minerals (%) Large minerals (%)
1 122.09 29.31 0.51 13.7 20.5 2.0 35.3 28.5 36.2 63.8
2 122.19 29.51 0.57 12.7 24.1 0.8 38.5 23.9 37.6 62.4
3 122.50 29.99 0.48 32.1 11.8 0.5 32.0 23.6 44.4 55.6
4 122.02 30.50 0.51 21.3 11.2 0.6 36.6 30.3 33.1 66.9
9 122.01 31.37 0.21 4.0 22.3 11.9 31.4 30.4 38.2 61.8
11 122.23 30.94 0.44 29.6 36.5 2.4 19.3 12.2 68.5 31.5
12 122.57 31.15 0.66 25.8 36.2 2.7 19.5 15.8 64.7 35.3
13 122.56 30.97 0.62 23.9 30.2 2.4 24.5 19.0 56.5 43.5
20 123.27 30.29 0.32 24.4 35.4 0.3 24.8 15.1 60.1 39.9
21 122.93 30.51 0.61 52.3 14.6 3.1 14.8 15.2 70.0 30.0
22 122.74 30.84 0.60 46.7 39.1 0.9 7.5 5.8 86.7 13.3
23 122.56 30.72 0.45 38.8 39.1 2.0 12.2 7.9 79.9 20.1
24 122.50 30.50 0.53 29.7 24.1 6.9 22.1 17.2 60.7 39.3
25 122.81 30.17 0.61 35.1 25.0 6.5 16.2 17.2 66.6 33.4
30 122.90 29.51 0.51 49.4 29.9 5.2 9.5 6.0 84.5 15.5
31 122.55 29.56 0.77 41.1 38.3 8.0 6.4 6.2 87.4 12.6
32 122.50 29.30 0.68 44.4 35.8 6.3 7.8 5.7 86.5 13.5
33 123.00 28.51 0.78 62.7 5.5 9.8 15.1 6.9 78.0 22.0
34 122.27 28.50 0.85 56.5 9.9 13.1 12.0 8.5 79.5 20.5
44 122.01 28.50 0.64 30.0 25.2 9.0 17.1 18.7 64.2 35.8
Table 2
Concentrations of different forms of P (mmol g
1
) (ExeP: exchangeable P; AueP:
authigenic P; DeeP: detrital P; OreP: organic P; ReeP: refractory P; FeeP: Fe-bound
P; TP: total P) in surface sediments from the Changjiang Estuary and adjacent ECS
inner shelf.
Sampling site ExeP AueP DeeP OreP ReeP FeeP TP
1 0.30 1.50 8.73 2.87 1.72 0.48 15.6
2 0.46 1.12 9.75 3.04 2.44 0.65 17.5
3 0.93 0.64 10.83 1.91 2.64 0.48 17.4
4 0.25 0.54 10.36 1.99 3.89 0.54 17.6
9 0.95 0.92 13.23 2.37 3.31 0.58 21.4
11 0.30 0.54 11.11 2.76 3.32 0.48 18.5
12 0.61 0.74 9.37 2.78 3.49 0.52 17.5
13 0.40 0.93 10.33 2.34 3.25 0.46 17.7
20 0.24 0.76 11.11 0.82 1.74 0.37 15.0
21 0.33 1.22 9.43 3.01 2.73 0.39 17.1
22 0.46 0.77 8.91 3.06 1.91 0.49 15.6
23 0.37 1.39 9.43 2.60 2.78 0.05 16.6
24 0.34 0.81 9.35 2.89 3.51 0.40 17.3
25 0.50 0.84 8.37 3.59 3.38 0.38 17.1
30 0.37 0.81 10.03 1.74 2.88 0.22 16.1
31 0.42 1.00 6.88 3.77 3.93 0.54 16.5
32 0.47 1.22 7.57 3.43 3.24 0.52 16.5
33 0.32 1.09 9.37 1.54 3.15 0.41 15.9
34 0.43 0.88 6.60 4.27 3.57 0.50 16.3
44 0.31 0.66 8.32 3.85 3.77 0.09 17.0
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 30
OreP and ReeP also accounted for a large proportion of TP in the
Changjiang LDE and adjacent coastal sediments. In contrast with
DeeP, Organic P (sum of OreP and ReeP) concentrations in this
study were generally higher than those from the intertidal sedi-
ments of the Changjiang LDE (Hou et al., 2009) and the ECS middle
shelf (Fang et al., 2007), but very close to those in the Arabian Sea
(Schenau and de Lange, 2001), and the Bohai and Yellow Seas (Liu
et al., 2004) (Fig. 3). Contributions of OreP and ReeP to TP were
5.5%e26.3% (16.1% 5.1%) and11.0%e23.8% (17.8% 3.6%),
respectively (Table 3). The fractions of Organic P in this study were
twice as much as those in intertidal sediments of the Changjiang
LDE and the ECS shelf regions (Fang et al., 2007; Hou et al., 2009; He
et al., 2009b). Higher contents of OreP were observed mainly in the
Changjiang LDE and ZheeMin coastal mud areas and were lower
near the river mouth and the outer shelf (Fig. 2d). Thus, OreP
showed a signicantly negative correlation with DeeP (r 0.71,
p < 0.001, n 20) (Fig. 3), and a positive correlation with ne-
grained sediments and related parameters, such as silt (r 0.51,
p < 0.05, n 20), clay (r 0.52, p < 0.05, n 20), TOC (r 0.52,
p < 0.05, n 20) and SSA (r 0.75, p < 0.001, n 20) (Fig. 4d), as
observed in other studies (Ruttenberg and Berner, 1993; Berner and
Rao, 1994; Rao and Berner, 1997; Schenau and de Lange, 2001; Liu
et al., 2004; Sutula et al., 2004; Fang et al., 2007; Hou et al., 2009).
The distribution pattern of ReeP was different from that of OreP
and DeeP in that higher contents of ReeP were not only found in
the ZheeMin coastal mud area, but also in areas near the river
mouth and the outer region of the Hangzhou Bay (Fig. 2e). Similarly,
ReeP also showed positive correlations with clay (r 0.62, p <0.01,
n 20), and kaolinite (r 0.56, p < 0.05, n 20) (Fig. 4e, f). As
mentioned earlier, these correlations were consistent with the fact
that organic matter is more easily bound with ne-grained sedi-
ments that have larger SSA, which results in more abundant TOC in
these muddy sediments. In addition, source differences among Ore
P, ReeP and DeeP were probably another cause for the heteroge-
neity of their distribution patterns. In addition to riverine input,
OreP is mainly derived from autochthonous marine primary pro-
duction (Jensen et al., 1995; Lukkari et al., 2009), coinciding with
the high productivity of the Changjiang diluted water (CJDW) and
the ZheeMin coast (Chen, 2008; Zhou et al., 2008). In contrast, Ree
P in the Changjiang was primarily composed of P associated with
clay minerals, e.g. aluminosilicate (Vink et al., 1997; Lukkari et a.,
2009), which supported the signicant relationship between Ree
P with clay and kaolinite (Al
4
[Si
4
O
10
]$(OH)
2
)in this study. The dis-
tribution of Organic P in this region is linked with the transport of
Fig. 2. Spatial distribution of different forms of phosphorus (a. ExeP: exchangeable P; b. AueP: authigenic P; c. DeeP: detrital P; d. OreP: organic P; e. ReeP: refractory P; f. FeeP:
Fe-bound P; g. TP: total P; h. BAP: bioavailable P) in surface sediments from the Changjiang Estuary and adjacent ECS inner shelf.
Fig. 3. DeeP and TOP bio-plot of surface sediments in the Changjiang Estuary and
adjacent ECS inner shelf and comparing with other estuaries and coastal margins
around the world such as the intertidal at of the Changjiang LDE (Hou et al., 2009),
Changjiang river mouth (Rao and Berner, 1997), middle shelf of the ECS (Fang et al.,
2007), Bohai and Yellow Sea (Liu et al., 2004), Amazon River and estuary (Berner
and Rao, 1994), Gulf of Mexico: shelf region (Ruttenberg and Berner, 1993), Arabian
Sea (Schenau and de Lange, 2001), and Mississippi River (Sutula et al., 2004). Data of
OreP in this study are also displayed (stars).
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 31
ne-grained sediments, which is controlled by the CJDW, coastal
currents and high primary productivity.
In the Changjiang Estuary sediments, fractions of AueP, ExeP
and FeeP in TP were relatively small, and the sum of their contri-
butions was only 10.5%. Despite having similar concentrations and
percentages, these three forms of P had totally different distribu-
tion patterns from each other, but were distinguishable from other
P forms. Among these three forms, the fraction of AueP was the
highest, ranging from 2.9 to 9.6% (average in 5.5%), next was ExeP
which accounted for 1.4e5.3% of TP (average in 2.5%), and the last
one was FeeP, varied from 0.3 to 3.7% (average in 2.5%)(Table 3).
The concentrations and percentages of AueP in this study were
generally lowcompared with other P forms, but very close to those
in intertidal sediments of the Changjiang LDE(6.3%) (Hou et al.,
2009), possibly because of the dilution effect of large amounts of
particulate matters transported by the Changjiang (Zheng et al.,
2003). The percentages of AueP in this study area were also com-
parable to those in the ECS middle shelf (5.8%) (Fang et al., 2007),
but much lower than those from the equatorial Pacic (61e86%),
where both organic matter degradation and Fe reduction rates
were relatively high and occurred deep in the sediment, thus
providing the necessary conditions for the phosphate concentra-
tions buildup and authigenic P formation (Filippelli and Delaney,
1996). AueP mainly includes authigenic carbonate uorapatite
(CFAP), biogenic apatite (i.e., bones, teeth, etc.), and carbonate-
associated P (Hou et al., 2009; Sekula-Wood et al., 2012). In this
region, there is a greater abundance biomass from siliceous than
calcareous organisms, resulting in very few calcium carbonate de-
posits (Zheng et al., 2003). Therefore, formation of AueP in this
region may be largely due to the authigenesis of CFAP, i.e. chemical
deposition of phosphate. Finally, post-depositional transformation
of P in sediments plays an important role in P cycles, by mediating
active P forms into inactive forms on the Changjiang LDE and the
ECS.
It has been generally accepted that the formation of authigenic
carbonates and CFAP occurs over long periods of time (e.g., thou-
sands to millions of years) and usually occurs in the deep sea
(Schuffertet al., 1994). However, recent studies have shown that in
LDEs such as the Amazon Delta, Gulf of Papua, and Aru Sea, remi-
neralization of OM is effectively enhanced by suboxic diagenetic
conditions, caused by frequently physical reworking of mobile
muds (Aller and Blair, 2004). Moreover, the formation of authigenic
minerals (e. g. authigenic carbonates and authigenic aluminosili-
cates) is greatly accelerated by reverse weathering processes,
thereby reducing the formation time from thousands or even mil-
lions of years, to only several years or decades (Michalopoulos and
Aller, 2004). The Changjiang LDE and ZheeMin coastal mud areas
were also characterized by suboxic redox conditions, signicant
remineralization of sedimentary OC and rapid formation of authi-
genic minerals (unpublished results). Therefore, it is likely that
rapid authigenic formation of AueP (especially CFAP) occurs in the
surface sediments of the Changjiang LDE. This is further supported
by the fact that the relatively high concentrations and percentages
of AueP and OreP were found mainly in the Changjiang LDE and
ZheeMin coastal mud areas (Fig. 2b and d).
The fraction of FeeP was small compared to all other P forms,
with an average of only 2.5%, much less than that of intertidal
sediments of the Changjiang LDE (w23.7%) (Hou et al., 2009),
surface sediments of Bohai and Yellow Seas (3e10%)(Liu et al.,
2004), Arabian Sea (w25%) (Schenau and de Lange, 2001) and
Florida Bay (w19%) (Zhang et al., 2004). The most abundant FeeP
was found in the Changjiang river mouth and the near-shore area of
the ZheeMin coast (Fig. 2f). As FeeP is formed by co-precipitation
of phosphate with Fe oxides/hydroxides, it can be easily desorbed
from host Fe-oxides/hydroxides under favorable environmental
conditions, such as reducing conditions in suboxic or anoxic zones
(Anschutz et al., 1998; Liu et al., 2004). As mentioned earlier, sed-
iments in the mud areas of the Changjiang Estuary and ZheeMin
coast were under suboxic conditions (unpublished results) when
we sampled, which partly explains why the fraction of FeeP in this
region was so low. Furthermore, with increasing pH and salinity as
transition from freshwaters to saline waters, there is a shift of the
speciation of phosphate from H
2
PO
4

to HPO
4
2
, and a change in the
surface charge on Fe oxides/hydroxides, which may inhibit phos-
phate adsorption onto Fe oxides/hydroxides (Hou et al., 2009).
Decreases in FeeP fractions in Changjiang LDE sediments were
observed along the salinity transect from 0.58 mmol g
1
at the river
mouth (site #9) to 0.37 mmol g
1
on the outer shelf (site #20)
(Table 2). This is similar to the Mississippi River Estuary, where the
percentages of FeeP were 40e46% of particulate P at 0 salinity,
while at salinities of 23e27, the FeeP also decreased to a non-
detectable amount (Sutula et al., 2004). Additionally, fresh/
brackish regions of an estuary, such as the intertidal ats of the
Changjiang Estuary (Xu et al., 2001; Hou et al., 2009), which have
been shown to have high concentrations of phosphates from large
inputs of municipal wastewaters and agricultural sources, may also
increase the adsorption of phosphate onto Fe oxides/hydroxides.
Past work shows that abundant particulate and colloidal iron
supplied from freshwater runoff and phosphorus from the decay of
seagrass tissues contributed to the relatively higher concentrations
of FeeP in the Florida Bay (Zhang et al., 2004). The concentrations
of total dissolved phosphate (TDP) in the Changjiang Estuary
decreased fromw2 mmol L
1
to w0.6 mmol L
1
fromthe head to the
mouth (He et al., 2009a), consistent with the tendency for FeeP
concentrations and fractions to decrease from the head to the
mouth of the estuary (Xu et al., 2001; Hou et al., 2009; He et al.,
2009b).
In contrast with FeeP, ExeP (also known as loosely-sorbed P) is
formed by direct adsorption of phosphate (in HPO
4
2
mainly) onto
mineral surfaces in sediments, thus ExeP can be utilized by living
organisms directly (Andrieux-Loyer and Aminot, 1997, and refer-
ences therein). In the Changjiang LDE, we found the fraction of Exe
P was also very low, with an average of only 2.5%. Similar with FeeP,
an obvious decrease of ExeP was observed along the salinity
transect from the river mouth to the outer shelf (Fig. 2a; Table 2).
Thus, the relatively high concentration of ExeP found at the
Table 3
Percent of different forms of P in TP (%) (TP: total P; ExeP: exchangeable P; AueP:
authigenic P; DeeP: detrital P; OreP: organic P; ReeP: refractory P; FeeP: Fe-bound
P) in surface sediments from the Changjiang Estuary and adjacent ECS inner shelf.
Sampling
site
ExeP (%) AueP (%) DeeP (%) OreP (%) ReeP (%) FeeP (%)
1 1.9 9.6 56.0 18.4 11.0 3.1
2 2.6 6.4 55.8 17.4 14.0 3.7
3 5.3 3.7 62.1 11.0 15.1 2.8
4 1.4 3.1 59.0 11.3 22.1 3.1
9 4.5 4.3 61.9 11.1 15.5 2.7
11 1.6 2.9 60.0 14.9 17.9 2.6
12 3.5 4.2 53.5 15.9 19.9 3.0
13 2.3 5.3 58.3 13.2 18.4 2.6
20 1.6 5.1 73.9 5.5 11.6 2.5
21 1.9 7.1 55.1 17.6 16.0 2.3
22 2.9 4.9 57.1 19.6 12.2 3.1
23 2.2 8.4 56.7 15.6 16.7 0.3
24 2.0 4.7 54.0 16.7 20.3 2.3
25 2.9 4.9 49.1 21.0 19.8 2.2
30 2.3 5.0 62.5 10.8 17.9 1.4
31 2.5 6.0 41.6 22.8 23.8 3.3
32 2.9 7.4 46.0 20.9 19.7 3.2
33 2.0 6.9 59.0 9.7 19.8 2.6
34 2.6 5.4 40.6 26.3 22.0 3.1
44 1.8 3.9 48.9 22.6 22.2 0.5
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 32
Changjiang river mouth and ZheeMin coast (Fig. 2a), may have
been caused by the high concentrations of phosphate inputs by the
Changjiang and along with inputs of coastal domestic sewage (Liu
et al., 2006b; Hou et al., 2009). Previous work has shown sub-
stantial competition for adsorption on mineral surfaces between
phosphate and anions (e.g. Cl

, SO
4
2
, OH

and Br

) (Hou et al.,
2009), which may help to explain the relatively higher concentra-
tions of ExeP in brackish waters compared to saline water areas in
the Changjiang LDE.
4.2. Phosphorus bioavailability in surface sediments
Enrichment of BAP in surface sediments may increase the
releasing potential of P from sediments to overlying water, espe-
cially when resuspension of sediments occurs from physical
reworking and/or from chemical drivers (e.g. pH, DO, ion concen-
trations, and surface charges) change. If there is P release, primary
productivity in overlying water and even upper water can be
enhanced (Andrieux-Loyer and Aminot, 1997; Coelho et al., 2004;
Hou et al., 2009). As mentioned previously, ExeP, OreP and Fe-P
in sediments can be easily released through physical, chemical
and/or biological reactions (Jensen and Thamdrup, 1993; Andrieux-
Loyer and Aminot, 1997; Rozan et al., 2002; Coelho et al., 2004;
Sutula et al., 2004; lvarez-Rogel et al., 2007; Hou et al., 2009), and
are recognized as potentially bioavailable P. The sum of these three
P forms (BAP) represents the upper limit of P that can be released
into overlying water (Andrieux-Loyer and Aminot, 1997; Hou et al.,
2009).
The BAP values in this study were comparable to previous
studies in the Changjiang LDE and the ECS continental shelf. For
example, the average concentrations and fractions of BAP in TP in
surface sediments of the Changjiang LDE and adjacent sea areas of
two surveys were 3.69 mmol g
1
and 22.1% (June 2006) and
3.49 mmol g
1
and 21.3% (April 2007), respectively (He et al.,
2009b).Fang et al. (2007) found that BAP accounted for about
29.7% of TP in the ECS middle shelf. However, when compared with
intertidal sediments of the Changjiang LDE and SPM in the
Changjiang main stream and estuary, BAP in surface sediments of
the Changjiang LDE were much lower for both absolute contents
and fractions in TP. BAP in intertidal sediments of the Changjiang
LDE ranged fromw3.7 to w22 mmol g
1
and accounted for 15.6%e
58.5% of TP, with signicant spatial and seasonal variations (Hou
et al., 2009). Furthermore, OreP was the major component of BAP
in the Changjiang Estuary sediments in this study, while in the
a
Fig. 4. Relationships between DeeP and clay (a), TOC (b), SSA (c), OreP and SSA(d), ReeP and clay (e), kaolinite (f) in surface sediments from the Changjiang Estuary and adjacent
ECS inner shelf.
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 33
intertidal sediments it has been shown that BAP was mainly
contributed by the form of Fe-bound P (Hou et al., 2009). These
results indicated that a considerable amount of BAP in estuarine
sediments/particles was decomposed and released into the water
column during transport and/or post-deposition processes.
Total particulate P concentration in SPM within the Changjiang
Estuary was w27 mmol g
1
and the concentrations of ExeP, OreP,
AueP, FeeP, ReeP and DeeP in SPM were 1.35, 7.42, 1.81, 1.00, 5.25
and 10.26 mmol g
1
, respectively (unpublished results). Compared
with sediments, the concentration and fraction of BAP in SPM were
relatively high (9.77 mmol g
1
and 36.1%), indicating the loss of BAP
as the SPM sedimented. In addition, release of FeeP, as mentioned
previously, is mainly controlled by redox conditions in sediments
(Andrieux-Loyer and Aminot, 1997; Hou et al., 2009). In mobile
muds of estuaries and marginal seas, frequent resuspension and
remobilization largely change the normal redox succession and
diagenetic ingrowth sequence in sediments, making Fe, Mn and
other redox sensitive elements experience repeated redox cycling
and releasing phosphate due to periodical reduction of Fe-bound P
(Aller and Blair, 2004; Coelho et al., 2004). This also explains why
the concentrations and percentages of FeeP in the estuaries and
marginal seas were much lower than those of intertidal sediments
(Hou et al., 2009). In contrast, phosphate can be gradually released
during the process of remineralization of OreP in the presence of
microorganisms (Andrieux-Loyer and Aminot, 1997). Suboxic
diagenetic conditions and abundant microbial diversity in the
sediments of estuaries and marginal seas promote the decompo-
sition of OM (including OreP), thereby enhancing the bioavail-
ability of OreP (Sutula et al., 2004). Phosphate concentrations in
overlying waters and sediment pore waters further support this
observation. For example, phosphate concentrations in overlying
waters of the mud areas (3.86 mmol L
1
and 2.11 mmol L
1
for site
#12 and #31, respectively) were much higher than those of the
non-mud areas (0.62 mmol L
1
for site #33) (unpublished results).
Similarly, the benthic ux of phosphate across sedimentewater
interface, estimated from the vertical distribution of phosphate in
pore waters, was 27.8 mmol m
2
yr
1
at site #12, and was two
times as large as that of site #33 (13.6 mmol m
2
yr
1
) (unpub-
lished results). Both the high concentrations and high uxes of
phosphate in the mud areas indicated the unique role of mobile-
muds in the release of BAP.
4.3. Preservation of phosphorus in surface sediments
TOC/SSA loadings is a parameter generally used to characterize
the preservation status of OC in sediments (Blair and Aller, 2012).
DepletedTOC/SSA loadings less than 0.40 mg C m
2
indicated sig-
nicant remineralization and low preservation efciency of TOC
sorbed on sediment surface, which is commonly found in either
highly dynamic deltaic mobile muds or in deep-sea deposits (Blair
and Aller, 2012). Here we use this general paradigm to discuss P/
SSA loading ratios and the preservation of different forms of P. The
physical meaning of P/SSA loading is dened as the binding strat-
egy of P with sediments through either adsorption or aggregation,
similar to that of TOC/SSA ratio. Although the distribution patterns
of different forms of P showed signicant spatial variations, dis-
tributions of different forms of P to SSA ratios were consistent with
each other (Table S2 and Fig. 5). In particular, the relatively high P/
SSA loadings were observed mainly in the Changjiang river mouth
(site #9) and relict sand areas off the estuary (site #20). Sites #30
and #33 also showed higher P/SSA ratios than the mud area sta-
tions. Lower ratios were found in the Changjiang Estuary and Zhee
Min coastal mud areas, with a similar distribution pattern of TOC/
SSA loadings (unpublished results), indicating the transformation
of different forms of P in these regions (Table S2; Fig. 5). Signicant
losses of labile and iron-bound P were also found from the lower
Mississippi River to the Gulf of Mexico due to physical reworking of
deposited riverine sediments on the continental shelf (Sutula et al.,
2004). This suggested that the preservation status of different P
forms was largely controlled by sedimentary environments and
sediment properties, and that low P preservation was associated
with highly dynamic muddy sediments.
As discussed earlier, when considering all six forms of P in this
study, only DeeP and OreP were signicantly correlated with SSA
(Fig. 4), indicating an apparent dependency between DeeP, OreP
and SSA. As shown in Fig. 4, DeeP decreased with an increase in
SSA, which we speculate may have been due to a dilution effect
and/or variation of mineral composition. It is also interesting to
note that OreP increased with increasing SSA, which was probably
attributed to absorption/aggregation of OM with minerals, consis-
tent with a dominant location of OreP on sediment surfaces.
However, DeeP/SSA, OreP/SSA loadings and SSA showed different
relationships. DeeP/SSA loadings decreased exponentially with the
increase of SSA, while OreP/SSA loadings varied very little with SSA
(Fig. 6c, d). Concentrations and fractions of DeeP in intertidal
sediments of the Changjiang Estuary and sandy areas of the middle
shelf of the ECS were much higher than in the ne-grained mud
areas of the estuary and coast (Fang et al., 2007; Hou et al., 2009).
Although there were no measured values of DeeP/SSA in those
areas prior to this work, higher DeeP/SSA loadings were expected,
considering their high DeeP and low SSA levels. Relationships be-
tween DeeP/SSA loadings and SSA indicated that DeeP had not
reached an equilibriumwith SSA, at least in the mud areas. Perhaps
an equilibrium between DeeP and SSA can be reached in the
southern part of the ZheeMin coastal mud area, but further studies
are needed to better understand the mechanisms involved.
AueP has relatively slow formation rate and its concentration is
low in estuarine and coastal sediments. Moreover, it is insoluble,
and thus not considered a primary source for P regeneration
(Andrieux-Loyer and Aminot, 1997; Hou et al., 2009). ReeP, as the
term suggests, is a P form that resists decomposition by
Fig. 5. Spatial distribution of SSA normalized TP in surface sediments from the
Changjiang Estuary and adjacent ECS inner shelf.
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 34
microorganisms, and is not available for algal growth (Vink et al.,
1997). Therefore, similar to DeeP, AueP and ReeP both belong to
the category of Immobile P (Imm-P), and consequently, the AueP/
SSA and ReeP/SSA loadings also decreased exponentially with in-
creases in SSA (Fig. 6b, e). The relationship between OreP/SSA and
SSA were quite different from those of DeeP/SSA, AueP/SSA and
ReeP/SSA. The maximum OreP/SSA loadings (0.68 mmol m
2
) in
these sediments occurred near the Changjiang River mouth (site
#9), which had the lowest SSAvalues (Table S2; Fig. 6d). The OreP/
SSA loadings at other sites basically remained unchanged with an
increase in SSA (Fig. 6d). Variation of OreP/SSA loadings versus SSA
indicated that OreP may have reached an adsorptionedesorption
equilibrium on mineral surfaces at most of our sampling sites e
even in relict sandy regions. Labile OreP appeared to have
decomposed sufciently, with no evidence of net loss and/or supply
during transport, which indicated that active P forms had relatively
higher turnover rates than other forms of P.
Similar to DeeP/SSA loadings, TOC/SSA loadings decreased (not
exponentially) with the increasing SSA (r 0.78, p < 0.001,
n 20) (Figure S1), which indicated that loss of TOC largely
occurred in sediments with higher SSA (unpublished results). This
difference indicated a preferential loss of OreP relative to OC.
Similar to OreP/SSA, ExeP/SSA also remained unchanged with
increasing SSA, except for several sites located in sandy areas,
which also indicated that ExeP had reached an adsorptione
desorption equilibrium with mineral surfaces, further supported
ExeP, as an active P form, had relatively higher turnover rates
(Fig. 6a). However, as a component of BAP, FeeP was different. Fee
P/SSAloadings decreased with the increasing SSAand changed very
little when SSA was higher than 15 m
2
g
1
, similar with AueP/SSA
and ReeP/SSA (both are Imm-P forms) (Fig. 6f). Changes in FeeP/
SSA with SSA were also consistent with the decreasing trends of
FeeP from intertidal wetlands to the Changjiang LDE and the ECS
shelf (Fang et al., 2007; Hou et al., 2009). Unlike ExeP and OreP,
FeeP was largely controlled by redox conditions in sediments, and
thus its equilibrium on mineral surfaces was difcult to achieve
(Anschutz et al., 1998; Liu et al., 2004). Since the redox conditions of
sediments were different from tidal wetlands of the Changjiang
LDE to the ECS shelf (Chen et al., 2007; Hou et al., 2009; unpub-
lished results), the variation of FeeP/SSA vs SSA should have also
been expected.
As previously mentioned, TOC/SSA and OreP/SSA loadings
changed inversely with SSA, implying different rates of decompo-
sition of TOC and OreP, and a preferential loss of OreP relative to
OC. The C/P ratios further supported this contention. Generally,
biogeochemical cycles of biogenetic elements, such as C, Nand P are
coupled with each other, and the relationships of these elements
can be and have been used, as indices of sources and/or the degree
of decomposition of OMin marine environments (Van der Zee et al.,
2002; Sekula-Wood et al., 2012). In the calculation of C/N/P stoi-
chiometry, total organic P (TOP, the sum of OreP and ReeP) is
usually employed (e.g., Ruttenberg and Goni, 1997; Hou et al.,
Fig. 6. Relationship between SSA and ExeP/SSA (a), AueP/SSA (b), DeeP/SSA (c), OreP/SSA (d), ReeP/SSA (e) and FeeP/SSA (f) in surface sediments from the Changjiang Estuary and
adjacent East China Sea shelf.
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 35
2009). TOC/TOP ratios of marine phytoplankton are usually close to
the Redeld ratio 106 (Redeld et al., 1963), while terrestrial plants
can have TOC/TOP ratios as high as 800e2050 (Van der Zee et al.,
2002, and references therein). Marine sediments have a wide
range of TOC/TOP ratios (50e4500) due to a mixture of marine and
terrestrial OM and/or regeneration of organic P (Anderson et al.,
2001). TOC/TOP ratios higher than the Redeld ratio (106) are
usually attributed to a dominance of terrestrial sources (Ruttenberg
and Goi, 1997), or preferential regeneration of P relative to C
(Ingall and Jahnke, 1997; Schenau and de Lange, 2001; Sekula-
Woodet al., 2012). TOC/TOP ratios less than the Redeld ratio
usually occurred in aerobic/suboxic areas characterized by lowTOC,
abundant refractory fractions in TOP, and/or a dominance of bac-
terial biomass (Ingall and Cappellen, 1990; Ruttenberg and Goi,
1997). In this study, TOC/TOP ratios of most sites were lower than
the Redeld ratio (84 in average), except one site fromthe ECS shelf
(138 in site #33) (Figure S2). These results were also lower than
those fromthe intertidal sediments of the Changjiang Estuary (Hou
et al., 2009) and other marginal seas, such as Mackenzie River and
shelf, Gulf of Mexico, Arabian Sea and Florida Bay (Ruttenberg and
Goi, 1997; Schenau and de Lange, 2001; Kang and Trefry, 2013),
but comparable to those found in the Amazon Shelf (Ruttenberg
and Goi, 1997). Unlike other marginal seas, efcient reminerali-
zation of OM in mobile muds of the Changjiang LDE (unpublished
results), Amazon shelf (Aller and Blair, 2006) (Fig. 7) and Gulf of
Papua (Aller and Blair, 2004) results in low abundance of TOC
(<1.0%) and thus low TOC/SSA loadings. Extensive physical
reworking of sediments occurring in these systems favors bacterial
growth by discouraging grazer colonization (Lee, 1992; Aller and
Stupakoff, 1996). In addition, as discussed previously, contribu-
tions of OreP and ReeP toTP in the Changjiang LDE sediments were
very close (16.1% and17.8% in average, respectively), indicating that
ReeP was an important component of TOP. These factors are
believed to be the reasons for such low TOC/TOP ratios in the
Changjiang LDE and other mobile-mud systems.
The occurrence of these special factors, especially the abundant
ReeP fractions unt TOC/TOP ratios for determination of prefer-
ential regeneration of P relative to C in mobile-muds. In fact, ReeP
fractions changed very little from SPM (19.4%) to sediments (17.8%)
in the Changjiang Estuary, while OreP fractions varied signicantly
(from 27.4% to 16.1%), suggesting signicant degradation of OreP
during transport. Since OreP is considered bioavailable and ReeP is
immobile and difcult to utilize (Vink et al., 1997; Lpez-Gutirrez
et al., 2004), it seems more reasonable to only include active OreP
in the calculation of C/P ratio. Therefore, TOC/OreP ratios were
calculated to test the preferential loss of P relative to C in this
system. As shown in Figure S2, the TOC/OreP ratios showed a
signicant correlation with TOC/TOP ratios (r 0.83, p < 0.001,
n 20), indicating high internal consistency between the variations
of these two ratios. In contrast with TOC/TOP ratios, TOC/OreP
ratios of most sites were higher than the Redeld ratio, except for
the site #9 (72) in the Changjiang river mouth (Fig. 8). TOC/OreP
ratios increased seaward from the estuary and reached the
maximum value of 422 in the deepest site #33 located in the ECS
shelf (Fig. 8). In fact, TOC to OreP ratios of SPM in the Changjiang
LDE were very close to the Redeld ratio (unpublished results), and
OMin sediments of the ECS shelf were mainly derived frommarine
sources (e.g. Xing et al., 2011; Li et al., 2012). Therefore, the low
TOC/SSA and OreP/SSA loadings and high TOC/OreP ratios in this
region not only indicated the occurrence of signicant reminerali-
zation of TOC and labile OreP in SPM and sediments during sedi-
mentation and remobilization, but also showed preferential loss of
OreP relative to OC during OM decomposition, as observed in the
eastern Arabian Sea (Babu and Nath, 2005). The TOC/OreP ratio in
sediment at site #20 (relict sand areas) was 324, consistent with its
low OreP/SSA loading, both indicated signicant decomposition of
OreP over OC. Thus, it appears that labile OreP has a faster turn-
over rate than OC in estuarine and coastal environments.
5. Conclusions
Concentrations and spatial distributions of P fractions in surface
sediments of the Changjiang LDE and adjacent ECS inner shelf re-
ected differences in sources and the preservation status of
different forms of P. DeeP was the major P form in surface
Fig. 7. TOC and TOP bio-plot of surface sediments in the Changjiang Estuary and
adjacent ECS inner shelf and comparing with other estuaries and coastal margins
around the world such as the intertidal at of the Changjiang LDE (Hou et al., 2009),
Mackenzie River and shelf, Gulf of Mexico (Mississippi LDE and Louisiana shelf) and
Amazon shelf (Ruttenberg and Goni, 1997), Arabian Sea (Schenau and de Lange, 2001),
and Florida Bay (Kang et al., 2013).
Fig. 8. Spatial distribution of TOC/OreP ratios in surface sediments from the Chang-
jiang Estuary and adjacent ECS inner shelf.
J. Meng et al. / Estuarine, Coastal and Shelf Science 144 (2014) 27e38 36
sediments, followed by ReeP and OreP, and these three P forms
accounted for 90% of TP. Similar with sandy sediments, high DeeP
values were primarily observed in the river mouth and outer shelf
regions off the Changjiang LDE. This indicated that riverine inputs
were the primary sources for DeeP. OreP showed a similar distri-
bution pattern with silt, SSA, and TOC, with higher values found in
the Changjiang LDE and ZheeMin coastal mud areas, indicating
that ne-grained sediments were the main carrier of OreP. DeeP in
this study was lower than those in the intertidal and middle-shelf
sediments, whereas TOP (sum of ReeP and OreP) was higher,
further suggesting that mobile muds were a sink of organic P. BAP
shared a similar distribution pattern with OreP, which was the
major component of BAP. BAP only accounted for w20% of TP in the
Changjiang LDE and adjacent ECS shelf, due to high concentrations
of DeeP. Comparison of P in surface sediments, overlying waters
and pore waters between mud areas and non-mud areas indicated
that suboxic diagenetic conditions promoted the decomposition of
OM in muddy sediments, thereby enhancing the bioavailability of
OreP. OreP/SSA loadings basically remained unchanged with the
increase of SSA in the Changjiang LDE and ZheeMin coastal mud
areas, implying sufcient decomposition of labile OreP and a
preferential loss of OreP relative to TOC during OM remineraliza-
tion processes e as further suggested by TOC/OreP ratios. The
distribution and the preservation of most P species seemed to be
predominantly controlled by physicochemical processes, such as
adsorptionedesorption reactions, physical reworking of mobile
muds, and redox conditions. This study highlights the potential
importance of the Changjiang LDE and ZheeMin coastal mud de-
posits in the decomposition and remobilization of P.
Acknowledgments
This work was partially supported by the National Natural Sci-
ence Foundation of China (Grant Nos. 40920164004, 41176063 and
41221004). We thank the crews of the R/V Runjiang 1, Hongtao
Chen, Hailong Zhang and Zongshan Zhao for sampling assistance.
Simin Fang is also appreciated for analytical supports. This is MCTL
contribution No. 28.
Appendix 2. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.ecss.2014.04.015.
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