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Speciation, bioavailability and preservation of phosphorus in surfacesediments of the Changjiang Estuary and adjacent East China Seainner 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, Chinab College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, Chinac Qingdao Collaborative Innovation Center of Marine Science and Technology, Qingdao 266100, China

d Institute of Marine Organic Geochemistry, Ocean University of China, Qingdao 266100, Chinae 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 2013Accepted 20 April 2014Available online 29 April 2014

Keywords:

phosphorousbiogeochemical cyclechemical speciationbioavailability

preservationsediments

a b s t r a c t

The speciation, potential bioavailability and preservation of phosphorus (P) in surface sediments of theChangjiang (Yangtze River) Estuary and adjacent East China Sea (ECS) inner shelf were investigatedthrough 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 (FeeP). Total P (TP) in surface sediments ranged from 15.0 to 21.4 mmol g1 and was highest near theChangjiang 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 higherconcentrations 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 theestuarine area and the ZheeMin coast. Bioavailable P (BAP), accounted for 9.5e32.0% of TP (with a meanof 21.2%) and showed a similar distribution pattern to that of OreP. DeeP/SSA and TOC/SSA loadings bothdecreased with increasing of SSA, while OreP/SSA loadings varied little with SSA, indicating that OrePmay 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 indicatedefcient remineralization of organic matter in mobile muds of the Changjiang Estuary and adjacent ECSinner shelf. Furthermore, the relatively high TOC/OreP ratios (72e422 with a mean of 188) likely suggesta 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 inbiogeochemical cycles of biogenic elements in estuarine andcoastal environments (Slomp, 2011), especially for large-riverdelta-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, marineautotrophic 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 islargely 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 mainlyfrom rivers) have slow formation kinetics, are buried directly andare slow to regenerate (Ruttenberg, 1992; Anschutz et al., 1998;Coelho et al., 2004). Signicant partitioning and transformation ofreactive P phases occur during burial processes driven by a numberof biological, physical, and geochemical processes (Schenau and deLange, 2001; Fang et al., 2007). The interactions of these complexbiogeochemical 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 atScienceDirect

Estuarine, Coastal and Shelf Science

j o u r n a l h o m e p a g e : w w w . e l s e v i e r .c o m / l o c a t e / e c ss

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

mailto:yaopeng@ouc.edu.cnmailto:pengyours@gmail.comhttp://www.sciencedirect.com/science/journal/02727714http://www.elsevier.com/locate/ecsshttp://dx.doi.org/10.1016/j.ecss.2014.04.015http://dx.doi.org/10.1016/j.ecss.2014.04.015http://dx.doi.org/10.1016/j.ecss.2014.04.015http://dx.doi.org/10.1016/j.ecss.2014.04.015http://dx.doi.org/10.1016/j.ecss.2014.04.015http://dx.doi.org/10.1016/j.ecss.2014.04.015http://www.elsevier.com/locate/ecsshttp://www.sciencedirect.com/science/journal/02727714http://crossmark.crossref.org/dialog/?doi=10.1016/j.ecss.2014.04.015&domain=pdfmailto:pengyours@gmail.commailto:yaopeng@ouc.edu.cn

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form of buried P (Ruttenberg, 1992; Andrieux-Loyer and Aminot,1997). For example, microbial breakdown of labile sedimentaryorganic matter (SOM) results in the release of phosphate, togetherwith dissolved organic phosphorus (DOP), nitrate, methane andcarbon dioxide, to the overlying water column where it is availablefor primary production (Andrieux-Loyer and Aminot, 1997). Theselinkages with marine primary productivity and sediment biogeo-chemical cycling, in part highlight the importance of studying thespeciation 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 ChangjiangRiver drainage basin has changed land-use practices which haspartly resulted in large increases in nutrient inputs to the Chang-

jiang LDE. Moreover, P has been shown to be a limiting nutrient forphytoplankton growth in the Changjiang LDE and the East ChinaSea (ECS) shelf (Liu et al., 2003). Thus, any increase in the release ofP from surface sediments to overlying waters could have a signi-cant impact on phytoplankton production and communitycomposition. As mentioned earlier, this release from sediments islargely 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 mainlyfocused on the distribution of P forms and their relationships withgrain size composition (Rao and Berner, 1997; He et al., 2009a) andbioavailability of particulate P (He et al., 2009b; Hou et al., 2009),with very few on the preservation of P (Fang et al., 2007). Inaddition, previous results either focused on the Changjiang Estuary(intertidal at)(Xuet al.,2001;Houet al.,2009) or fromfurther off-shore (middle shelf) (Zheng et al., 2003; Fang et al., 2007) in theECS, with very few on the outer estuary and inner shelf regions (Heet al., 2009b). More specically, studies on the unique roles of muddeposits in determining the source and fate of different forms of Pin 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, distribution patterns, potential

bioavailability and preservation of different forms of P, and theireffects on the Changjiang LDE and the ECS inner shelf, withparticular emphasis on the mobile-mud belts. The primary goal ofthis work was to better constrain the biogeochemical processes in Pcycling 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, rankedthird in

length (6300 km), fth in freshwater discharge (9.0 1011

m3

yr1

),and fourth in sediment discharge (4.8 108 t yr1) in the world(Dagg et al., 2004). The Changjiang LDE is characterized by highproductivity that largely stems from the high amounts of nutrientsdischarged by the river (Zhou et al., 2008). An increase in theloading of nutrients has also caused severe eutrophication in theChangjiang LDE, resulting in the frequent occurrence of harmfulalgal 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 thenutrient structure, rather than simply high nutrient loadings (Jianget al., 2010).

The hydrographic regimes of the Changjiang LDE and the ECSinner shelf are very complex and are mainly controlled by the

Yellow Sea Coastal Current (YSCC) in the north, the Zhee

Min

Coastal Current (ZMCC), and the Taiwan Warm Current (TWWC) inthe southeas well as the Changjiang Diluted Water (CJDW) (Fig.1)(Liu et al., 2007). All of the aforementioned currents play a key rolein 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 sedimentationrates ranging from 1 to 6 cm yr1(Guo et al., 2003; Liu et al., 2007).Much of the remaining sediment is transported southward alongthe ZheeMin coast by the CJDW and littoral currents (YSCC andZMCC), where it is deposited west of 123E due to a barrier and/orshear 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 thenortheast of the estuary in summer due to enhanced northeast-ward ow of the CJDW and TWWC (Liu et al., 2006b).

Sampling was conducted onboard theR/V Runjiang 1(ZhoushanRunhe Co., Ltd., China) from late July to early August in 2011 (Fig.1).Surface sediment samples (approx. 5 cm) were collected using astainless-steel box-corer in the Changjiang LDE and the ECS innershelf. 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 mudareas.

2.2. Analyses of sediment grain size, surface area and mineral

composition

Grain size composition of the samples was measured using alaser particle size analyzer (Mastersizer 2000, Malven InstrumentsLtd., UK), following the method ofHu 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.)

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adsorption surface area analyzer (3H-2000BET-A, BeishideInstrument-ST Co., Ltd., China), according toWaterson and Canuel(2008).

The bulk mineralogical composition of the surface sedimentswas determined using a Bruker D8 Advance X-Ray. Diffractometer(XRD) equipped with a copper anode (40 kV, 40 mA) after grindingand homogenization of samples to

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in the mud areas, while ReeP was mainly distributed throughoutthe 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 Pforms mentioned above (Table 2).

4. Discussion

4.1. Phosphorus speciation in surface sediments

In general, DeeP concentrations in this study were lower thanthose from intertidal sediments of the Changjiang LDE (Hou et al.,2009) and middle shelf of the ECS (Fang et al., 2007), but werehigher than other estuaries and marginal seas, such as the ArabianSea (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). DeePaccounted 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 andadjacent areas (51.2%) (He et al., 2009b). However, our DeeP waslower than those found in the middle shelf of the ECS (70.4%) byFang et al. (2007)and the Changjiang river mouth (64%) (Rao andBerner, 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 bysandy sediments, and the fractions of DeeP in TP reached 61.9% and73.9%, respectively (Table 3). Similarly, the DeeP fractions found inthe Changjiang LDE were higher than other estuaries and marginalseas around the world at the similar TP levels (Table 3). Forexample, DeeP accounted for only about 6% of TP in the AmazonEstuary (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, andthe Yellow Sea of China were all characterized by high DeeP con-tributions(Liu et al., 2004), similar to the Changjiang LDE. Onepossible explanation for these differences is that eroded soils fromthe upper basins of the Changjiang and Yellow Rivers transportedby the rivers to the Eastern Marginal Seas of China are enriched inDeeP, whereas rivers like the Amazon, which mainlyows throughtropical rain forests, tropical grasslands and alpine plant regions(with fertile soils), have a more limited DeeP contribution (Bernerand Rao, 1994; Liu et al., 2006a). This concept is supported by thehigh concentrations and percentages of DeeP in suspended par-ticulate matters (SPM) of the Yellow River 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) andSSA (r 0.78,p < 0.001,n 20) (Fig. 4a, b, c). These correlationscan be attributed to the fact that DeeP is mainly composed byprimary minerals, such as quartz and feldspar, which are the majorcomponents of coarse silt, sand and other sediments that have alarge particle size, small-SSA and low-TOC (Keil et al.,1997). Quartzand 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 sedimentsin the Changjiang LDE and adjacent areas (using a water elutriationmethod (He et al., 2009b)), showed that larger hydrodynamic sizes(32e63 mm and >63 mm) were also associated with higher con-

centrations and percentages of Dee

P.

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 63.82 122.19 29.51 0.57 12.7 24.1 0.8 38.5 23.9 37.6 62.43 122.50 29.99 0.48 32.1 11.8 0.5 32.0 23.6 44.4 55.64 122.02 30.50 0.51 21.3 11.2 0.6 36.6 30.3 33.1 66.99 122.01 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 31.512 122.57 31.15 0.66 25.8 36.2 2.7 19.5 15.8 64.7 35.313 122.56 30.97 0.62 23.9 30.2 2.4 24.5 19.0 56.5 43.520 123.27 30.29 0.32 24.4 35.4 0.3 24.8 15.1 60.1 39.921 122.93 30.51 0.61 52.3 14.6 3.1 14.8 15.2 70.0 30.022 122.74 30.84 0.60 46.7 39.1 0.9 7.5 5.8 86.7 13.323 122.56 30.72 0.45 38.8 39.1 2.0 12.2 7.9 79.9 20.124 122.50 30.50 0.53 29.7 24.1 6.9 22.1 17.2 60.7 39.325 122.81 30.17 0.61 35.1 25.0 6.5 16.2 17.2 66.6 33.430 122.90 29.51 0.51 49.4 29.9 5.2 9.5 6.0 84.5 15.531 122.55 29.56 0.77 41.1 38.3 8.0 6.4 6.2 87.4 12.632 122.50 29.30 0.68 44.4 35.8 6.3 7.8 5.7 86.5 13.533 123.00 28.51 0.78 62.7 5.5 9.8 15.1 6.9 78.0 22.034 122.27 28.50 0.85 56.5 9.9 13.1 12.0 8.5 79.5 20.544 122.01 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 g1) (ExeP: exchangeable P; AueP:authigenic P; DeeP: detrital P; OreP: organic P; ReeP: refractory P; FeeP: Fe-boundP; TP: total P) in surface sediments from the Changjiang Estuary and adjacent ECSinner shelf.

Sampling site ExeP AueP DeeP OreP ReeP FeeP TP

1 0.30 1.50 8.73 2.87 1.72 0.48 15.62 0.46 1.12 9.75 3.04 2.44 0.65 17.53 0.93 0.64 10.83 1.91 2.64 0.48 17.44 0.25 0.54 10.36 1.99 3.89 0.54 17.69 0.95 0.92 13.23 2.37 3.31 0.58 21.411 0.30 0.54 11.11 2.76 3.32 0.48 18.512 0.61 0.74 9.37 2.78 3.49 0.52 17.513 0.40 0.93 10.33 2.34 3.25 0.46 17.720 0.24 0.76 11.11 0.82 1.74 0.37 15.021 0.33 1.22 9.43 3.01 2.73 0.39 17.122 0.46 0.77 8.91 3.06 1.91 0.49 15.623 0.37 1.39 9.43 2.60 2.78 0.05 16.624 0.34 0.81 9.35 2.89 3.51 0.40 17.325 0.50 0.84 8.37 3.59 3.38 0.38 17.130 0.37 0.81 10.03 1.74 2.88 0.22 16.131 0.42 1.00 6.88 3.77 3.93 0.54 16.532 0.47 1.22 7.57 3.43 3.24 0.52 16.533 0.32 1.09 9.37 1.54 3.15 0.41 15.934 0.43 0.88 6.60 4.27 3.57 0.50 16.344 0.31 0.66 8.32 3.85 3.77 0.09 17.0

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OrePandReeP alsoaccounted for a large proportion of TP in theChangjiang LDE and adjacent coastal sediments. In contrast withDeeP, Organic P (sum of OreP and ReeP) concentrations in thisstudy were generally higher than those from the intertidal sedi-

ments of the Changjiang LDE (Hou et al., 2009) and the ECS middleshelf (Fang et al., 2007), but very close to those in the Arabian Sea(Schenau and de Lange, 2001), and the Bohai and Yellow Seas (Liuet al., 2004)(Fig. 3). Contributions of OreP and ReeP to TP were5.5%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 weretwice as much as those in intertidal sediments of the ChangjiangLDE and the ECS shelf regions (Fang et al., 2007; Hou et al., 2009; Heet al., 2009b). Higher contents of OreP wereobserved mainly in theChangjiang LDE and ZheeMin coastal mud areas and were lowernear the river mouth and the outer shelf (Fig. 2d). Thus, OrePshowed 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

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ne-grained sediments, which is controlled by the CJDW, coastalcurrents and high primary productivity.

In the Changjiang Estuary sediments, fractions of AueP, ExePand FeeP in TP were relatively small, and the sum of their contri-butions was only 10.5%. Despite having similar concentrations andpercentages, these three forms of P had totally different distribu-tion patterns from each other, but were distinguishable from otherP forms. Among these three forms, the fraction of AueP was thehighest, ranging from 2.9 to 9.6% (average in 5.5%), next was ExePwhich accounted for 1.4e5.3% of TP (average in 2.5%), and the lastone 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 low compared with other P forms, but very close to thosein intertidal sediments of the Changjiang LDE(6.3%) (Hou et al.,2009), possibly because of the dilution effect of large amounts ofparticulate 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 rateswere relatively high and occurred deep in the sediment, thusproviding 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 thancalcareous organisms, resulting in very few calcium carbonate de-posits (Zheng et al., 2003). Therefore, formation of AueP in thisregion may be largely due to the authigenesis of CFAP, i.e. chemicaldeposition of phosphate. Finally, post-depositional transformationof P in sediments plays an important role in P cycles, by mediatingactive P forms into inactive forms on the Changjiang LDE and theECS.

It has been generally accepted that the formation of authigeniccarbonates 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 inLDEs 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 authigenicminerals (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 andAller, 2004). The Changjiang LDE and ZheeMin coastal mud areaswere also characterized by suboxic redox conditions, signicantremineralization of sedimentary OC and rapid formation of authi-genic minerals (unpublished results). Therefore, it is likely thatrapid authigenic formation of AueP (especially CFAP) occurs in thesurface sediments of the Changjiang LDE. This is further supportedby the fact that the relatively high concentrations and percentagesof AueP and OreP were found mainly in the Changjiang LDE andZheeMin 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 intertidalsediments 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) andFlorida Bay (w19%) (Zhang et al., 2004). The most abundant FeePwas found in the Changjiang river mouth and the near-shore area ofthe ZheeMin coast (Fig. 2f). As FeeP is formed by co-precipitation

of phosphate with Fe oxides/hydroxides, it can be easily desorbedfrom host Fe-oxides/hydroxides under favorable environmentalconditions, 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 ZheeMincoast were under suboxic conditions (unpublished results) whenwe sampled, which partly explains why the fraction of FeeP in thisregion was so low. Furthermore, with increasing pH and salinity astransition from freshwaters to saline waters, there is a shift of thespeciation of phosphate from H2PO4

to HPO42, 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 wereobserved along the salinity transect from 0.58mmol g1 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 thepercentages 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 theChangjiang Estuary (Xu et al., 2001; Hou et al., 2009), which havebeen shown to have high concentrations of phosphates from largeinputs of municipal wastewaters and agricultural sources, may alsoincrease the adsorption of phosphate onto Fe oxides/hydroxides.Past work shows that abundant particulate and colloidal ironsupplied from freshwater runoff and phosphorus from the decay ofseagrass tissues contributed to the relatively higher concentrationsof FeeP in the Florida Bay (Zhang et al., 2004). The concentrations

of total dissolved phosphate (TDP) in the Changjiang Estuarydecreased fromw2 mmol L1 tow0.6 mmolL1 fromthe head tothemouth (He et al., 2009a), consistent with the tendency for FeePconcentrations and fractions to decrease from the head to themouth 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) isformed by direct adsorption of phosphate (in HPO42 mainly) ontomineral surfaces in sediments, thus ExeP can be utilized by livingorganisms directly (Andrieux-Loyer and Aminot, 1997, and refer-ences therein). In the Changjiang LDE, we found the fraction of ExeP was alsoverylow, with an average of only 2.5%. Similar with FeeP,an obvious decrease of ExeP was observed along the salinitytransect from the river mouth to the outer shelf (Fig. 2a;Table 2).

Thus, the relatively high concentration of Exe

P 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-boundP) in surface sediments from the Changjiang Estuary and adjacent ECS inner shelf.

Samplingsite

ExeP (%) AueP (%) DeeP (%) OreP (%) ReeP (%) FeeP (%)

1 1.9 9.6 56.0 18.4 11.0 3.12 2.6 6.4 55.8 17.4 14.0 3.7

3 5.3 3.7 62.1 11.0 15.1 2.84 1.4 3.1 59.0 11.3 22.1 3.19 4.5 4.3 61.9 11.1 15.5 2.711 1.6 2.9 60.0 14.9 17.9 2.612 3.5 4.2 53.5 15.9 19.9 3.013 2.3 5.3 58.3 13.2 18.4 2.620 1.6 5.1 73.9 5.5 11.6 2.521 1.9 7.1 55.1 17.6 16.0 2.322 2.9 4.9 57.1 19.6 12.2 3.123 2.2 8.4 56.7 15.6 16.7 0.324 2.0 4.7 54.0 16.7 20.3 2.325 2.9 4.9 49.1 21.0 19.8 2.230 2.3 5.0 62.5 10.8 17.9 1.431 2.5 6.0 41.6 22.8 23.8 3.332 2.9 7.4 46.0 20.9 19.7 3.233 2.0 6.9 59.0 9.7 19.8 2.634 2.6 5.4 40.6 26.3 22.0 3.144 1.8 3.9 48.9 22.6 22.2 0.5

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Changjiang river mouth and ZheeMin coast (Fig. 2a), may havebeen caused by the high concentrations of phosphate inputs by theChangjiang and along with inputs of coastal domestic sewage (Liuet al., 2006b; Hou et al., 2009). Previous work has shown sub-stantial competition for adsorption on mineral surfaces betweenphosphate and anions (e.g. Cl, SO4

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 inthe Changjiang LDE.

4.2. Phosphorus bioavailability in surface sediments

Enrichment of BAP in surface sediments may increase thereleasing potential of P from sediments to overlying water, espe-cially when resuspension of sediments occurs from physicalreworking and/or from chemical drivers (e.g. pH, DO, ion concen-trations, and surface charges) change. If there is P release, primaryproductivity in overlying water and even upper water can beenhanced (Andrieux-Loyer and Aminot, 1997; Coelho et al., 2004;Hou et al., 2009). As mentioned previously, ExeP, OreP and Fe-Pin sediments can be easily released through physical, chemicaland/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), andare recognized as potentially bioavailable P. The sum of these threeP forms (BAP) represents the upper limit of P that can be releasedinto overlying water (Andrieux-Loyer and Aminot, 1997; Hou et al.,2009).

The BAP values in this study were comparable to previousstudies in the Changjiang LDE and the ECS continental shelf. Forexample, the average concentrations and fractions of BAP in TP insurface sediments of the Changjiang LDE and adjacent sea areas oftwo surveys were 3.69 mmol g1 and 22.1% (June 2006) and3.49 mmol g1 and 21.3% (April 2007), respectively (He et al.,2009b).Fang et al. (2007) found that BAP accounted for about29.7% of TP in the ECS middle shelf. However, when compared withintertidal sediments of the Changjiang LDE and SPM in theChangjiang main stream and estuary, BAP in surface sediments ofthe Changjiang LDE were much lower for both absolute contentsand fractions in TP. BAP in intertidal sediments of the ChangjiangLDE ranged fromw3.7 tow22mmol g1 and accounted for 15.6%e58.5% of TP, with signicant spatial and seasonal variations (Houet al., 2009). Furthermore, OreP was the major component of BAPin 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.

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intertidal sediments it has been shown that BAP was mainlycontributed by the form of Fe-bound P (Hou et al., 2009). Theseresults indicated that a considerable amount of BAP in estuarinesediments/particles was decomposed and released into the watercolumn during transport and/or post-deposition processes.

Total particulate P concentration in SPM within the ChangjiangEstuary was w27mmol g1 and the concentrations of ExeP, OreP,AueP, FeeP, ReeP and DeeP in SPM were 1.35, 7.42, 1.81,1.00, 5.25and 10.26mmol g1, respectively (unpublished results). Comparedwith sediments, the concentration and fraction of BAP in SPM wererelatively high (9.77 mmol g1 and 36.1%), indicating the loss of BAPas the SPM sedimented. In addition, release of FeeP, as mentionedpreviously, is mainly controlled by redox conditions in sediments(Andrieux-Loyer and Aminot, 1997; Hou et al., 2009). In mobilemuds of estuaries and marginal seas, frequent resuspension andremobilization largely change the normal redox succession anddiagenetic ingrowth sequence in sediments, making Fe, Mn andother redox sensitive elements experience repeated redox cyclingand releasing phosphate due to periodical reduction of Fe-bound P(Aller and Blair, 2004; Coelho et al., 2004). This also explains whythe concentrations and percentages of FeeP in the estuaries andmarginal seas were much lower than those of intertidal sediments

(Hou et al., 2009). In contrast, phosphate can be gradually releasedduring the process of remineralization of OreP in the presence ofmicroorganisms (Andrieux-Loyer and Aminot, 1997). Suboxicdiagenetic conditions and abundant microbial diversity in thesediments 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 inoverlying waters and sediment pore waters further support thisobservation. For example, phosphate concentrations in overlyingwaters of the mud areas (3.86 mmol L1 and 2.11mmol L1 for site#12 and #31, respectively) were much higher than those of thenon-mud areas (0.62mmol L1 for site #33) (unpublished results).Similarly, the benthic ux of phosphate across sedimentewaterinterface, estimated from the vertical distribution of phosphate in

pore waters, was 27.8 mmol m

2 yr

1 at site #12, and was twotimes as large as that of site #33 (13.6 mmol m2 yr1) (unpub-lished results). Both the high concentrations and high uxes ofphosphate 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 characterizethe preservation status of OC in sediments (Blair and Aller, 2012).DepletedTOC/SSA loadings less than 0.40 mg C m2 indicated sig-nicant remineralization and low preservation efciency of TOCsorbed on sediment surface, which is commonly found in eitherhighly 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. Thephysical 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 patternsof different forms of P showed signicant spatial variations, dis-tributions of different forms of P to SSA ratios were consistent witheach other (Table S2andFig. 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 #30and #33 also showed higher P/SSA ratios than the mud area sta-tions. Lower ratios were found in the Changjiang Estuary and ZheeMin 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). Signi

cant

losses of labile and iron-bound P were also found from the lowerMississippi River to the Gulf of Mexico due to physical reworking ofdeposited riverine sediments on the continental shelf (Sutula et al.,2004). This suggested that the preservation status of different Pforms was largely controlled by sedimentary environments andsediment properties, and that low P preservation was associatedwith highly dynamic muddy sediments.

As discussed earlier, when considering all six forms of P in thisstudy, only DeeP and OreP were signicantly correlated with SSA(Fig. 4), indicating an apparent dependency between DeeP, OrePand SSA. As shown inFig. 4, DeeP decreased with an increase inSSA, which we speculate may have been due to a dilution effectand/or variation of mineral composition. It is also interesting tonote that OreP increased with increasing SSA, which was probablyattributed 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 differentrelationships. DeeP/SSA loadings decreased exponentially with theincrease of SSA, while OreP/SSA loadings varied very little with SSA(Fig. 6c, d). Concentrations and fractions of DeeP in intertidalsediments of the Changjiang Estuary and sandy areas of the middle

shelf of the ECS were much higher than in the ne-grained mudareas of the estuary and coast (Fang et al., 2007; Hou et al., 2009).Although there were no measured values of DeeP/SSA in thoseareas 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 notreached an equilibrium with SSA, at least in the mud areas. Perhapsan equilibrium between DeeP and SSA can be reached in thesouthern part of the ZheeMin coastal mud area, but further studiesare needed to better understand the mechanisms involved.

AueP has relatively slow formation rate and its concentration islow 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.

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microorganisms, and is not available for algal growth (Vink et al.,1997). Therefore, similar to DeeP, AueP and ReeP both belong tothe category ofImmobile 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 andSSA were quite different from those of DeeP/SSA, AueP/SSA andReeP/SSA. The maximum OreP/SSA loadings (0.68 mmol m2) inthese 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 anincrease in SSA (Fig. 6d). Variation of OreP/SSA loadings versus SSA

indicated that OreP may have reached an adsorptionedesorptionequilibrium on mineral surfaces at most of our sampling sites eeven in relict sandy regions. Labile OreP appeared to havedecomposed sufciently, with no evidence of net loss and/orsupplyduring transport, which indicated that active P forms had relativelyhigher turnover rates than other forms of P.

Similar to DeeP/SSA loadings, TOC/SSA loadings decreased (notexponentially) with the increasing SSA (r 0.78, p < 0.001,n 20) (Figure S1), which indicated that loss of TOC largelyoccurred in sediments with higher SSA (unpublished results). Thisdifference indicated a preferential loss of OreP relative to OC.Similar to OreP/SSA, ExeP/SSA also remained unchanged withincreasing SSA, except for several sites located in sandy areas,which also indicated that ExeP had reached an adsorptionedesorption 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. FeeP/SSA loadings decreased with the increasing SSAand changed verylittle when SSA was higher than 15 m2 g1, similar with AueP/SSAand ReeP/SSA (both are Imm-P forms) (Fig. 6f). Changes in FeeP/SSA with SSA were also consistent with the decreasing trends ofFeeP from intertidal wetlands to the Changjiang LDE and the ECSshelf (Fang et al., 2007; Hou et al., 2009). Unlike ExeP and OreP,FeeP was largely controlled by redox conditions in sediments, andthus 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 ChangjiangLDE to the ECS shelf (Chen et al., 2007; Hou et al., 2009; unpub-lished results), the variation of FeeP/SSA vs SSA should have alsobeen expected.

As previously mentioned, TOC/SSA and OreP/SSA loadingschanged inversely with SSA, implying different rates of decompo-sition of TOC and OreP, and a preferential loss of OreP relative toOC. The C/P ratios further supported this contention. Generally,biogeochemical cycles of biogenetic elements,such as C, N and P arecoupled with each other, and the relationships of these elementscan be and have been used, as indices of sources and/or the degreeof decomposition of OM in 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) isusually 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.

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2009). TOC/TOP ratios of marine phytoplankton are usually close tothe Redeld ratio 106 (Redeld et al.,1963), while terrestrial plantscan have TOC/TOP ratios as high as 800e2050 (Van der Zee et al.,2002, and references therein). Marine sediments have a widerange of TOC/TOP ratios (50e4500) due to a mixture of marine andterrestrial OM and/or regeneration of organic P (Anderson et al.,2001). TOC/TOP ratios higher than the Redeld ratio (106) areusually attributed to a dominance of terrestrial sources (Ruttenbergand 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 ratiousually occurred in aerobic/suboxic areascharacterized by low TOC,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 thanthe Redeld ratio (84 in average), except one site from the ECS shelf(138 in site #33) (Figure S2). These results were also lower thanthose from the intertidal sediments of the Changjiang Estuary (Houet al., 2009) and other marginal seas, such as Mackenzie River andshelf, Gulf of Mexico, Arabian Sea and Florida Bay (Ruttenberg andGoi, 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 (unpublishedresults), Amazon shelf (Aller and Blair, 2006)(Fig. 7) and Gulf ofPapua (Aller and Blair, 2004) results in low abundance of TOC(

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sediments, followed by ReeP and OreP, and these three P formsaccounted for 90% of TP. Similar with sandy sediments, high DeePvalues were primarily observed in the river mouth and outer shelfregions off the Changjiang LDE. This indicated that riverine inputswere the primary sources for DeeP. OreP showed a similar distri-bution pattern with silt, SSA, and TOC, with higher values found inthe Changjiang LDE and ZheeMin coastal mud areas, indicatingthat ne-grained sediments were the main carrier of OreP. DeeP inthis study was lower than those in the intertidal and middle-shelfsediments, whereas TOP (sum of ReeP and OreP) was higher,further suggesting that mobile muds were a sink of organic P. BAPshared a similar distribution pattern with OreP, which was themajor component of BAP. BAP only accounted forw20% of TP in theChangjiang LDE and adjacent ECS shelf, due to high concentrationsof DeeP. Comparison of P in surface sediments, overlying watersand pore waters between mud areas and non-mud areas indicatedthat suboxic diagenetic conditions promoted the decomposition ofOM in muddy sediments, thereby enhancing the bioavailability ofOreP. OreP/SSA loadings basically remained unchanged with theincrease of SSA in the Changjiang LDE and ZheeMin coastal mudareas, implying sufcient decomposition of labile OreP and apreferential loss of OreP relative to TOC during OM remineraliza-

tion processes e as further suggested by TOC/OreP ratios. Thedistribution and the preservation of most P species seemed to bepredominantly controlled by physicochemical processes, such asadsorptionedesorption reactions, physical reworking of mobilemuds, and redox conditions. This study highlights the potentialimportance 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 and41221004). We thank the crews of the R/V Runjiang 1, HongtaoChen, Hailong Zhang and Zongshan Zhao for sampling assistance.

Simin Fang is also appreciated for analytical supports. This is MCTLcontribution 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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