Marine Pollution Bulletin xxx (2015) xxx–xxx

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Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea Bin Yang a,b, Lu Cao a,c, Su-Mei Liu a,⇑, Guo-Sen Zhang d a Key Laboratory of Marine Chemistry Theory and Technology, Ocean University of China, Ministry of Education/Qingdao Collaborative Innovation Center of Marine Science and Technology, Qingdao 266100, China b Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Qinzhou University, Qinzhou 535099, China c Shandong Provincial Key Laboratory of Ocean Environment Monitoring Technology, Shandong Academy of Sciences Institute of Oceanographic Instrumentation, Qingdao 266001, China d State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China

a r t i c l e

i n f o

Article history: Received 14 November 2014 Revised 12 April 2015 Accepted 2 May 2015 Available online xxxx Keywords: Biogenic elements Biogeochemical cycling Surface sediments Yangtze River Estuary East China Sea

a b s t r a c t This study investigated the distribution and roles of total organic carbon (TOC), biogenic silicon (BSi), various forms of nitrogen (N) and phosphorus (P), and the stable carbon isotope (d13C) in surface sediments of the Yangtze River Estuary (YRE) and adjacent sea. Terrestrial input accounted for 12–63% of total organic matter in the study area. The distribution of biogenic elements was affected by the Changjiang Diluted Water, the Jiangsu Coastal Current, human activities, marine biological processes, and the sediment grain size. Potentially bioavailable N and P accounted for an average 79.6% of the total N (TN) and 31.8% of the total P (TP), respectively. The burial fluxes for TOC, BSi, TN and TP were 39.74–2194.32, 17.34–517.48, 5.02–188.85 and 3.10–62.72 lmol cm2 yr1, respectively. The molar ratios of total N/P (1.2–5.0), Si/P (5.0–14.8) and Fe/P (21–61) indicated that much of the P was sequestered in sediments. Ó 2015 Published by Elsevier Ltd.

Larger river-dominated coastal margins are active interfaces between terrestrial and oceanic environments, and are subject to large discharges of riverine materials, anthropogenic inputs and complex biogeochemical processes (Bianchi and Allison, 2009). As >80% of global burial of organic carbon happens in these shallow marine systems, the sedimentary organic matter in estuarine–shelf regions plays a significant role in the context of the global carbon cycle (Hedges and Keil, 1995; Tesi et al., 2007). Nitrogen (N), phosphorus (P) and silicon (Si) are primary nutrients, and play important roles in the biogeochemical cycling of biogenic elements in estuaries and continental shelves (Liu et al., 2005a; Falco et al., 2010; Slomp, 2011). Thus, an investigation of total organic carbon (TOC), biogenic silicon (BSi), and various N and P forms in marine sediments is essential for evaluating the response of aquatic ecosystems to global climate and environmental changes, and the impacts of human activities (De Lange, 1992; Schenau and De Lange, 2001; Krom et al., 2004; Liu et al., 2004; Yu et al., 2012b). The Yangtze River (Changjiang) Estuary (YRE) and the adjacent inner shelf of the East China Sea (ECS) form one of the largest estuarine–shelf systems in the world, and annually receive huge quantities of particulate matter transported by the Yangtze River ⇑ Corresponding author. E-mail address: [email protected] (S.-M. Liu).

(Milliman et al., 1985). The rapid economy development in the Yangtze River catchment has resulted in excessive nutrient discharge and changes in relative nutrient concentrations. This has had many detrimental impacts on aquatic ecosystems of the YRE and adjacent sea (Chai et al., 2006; Zhou et al., 2008; Zhu et al., 2011b), including eutrophication, harmful algal blooms, and seasonal hypoxia in bottom waters. Most previous studies of the sedimentary organic matter and biogenic elements of the YRE and adjacent shelf have focused on the concentration and distribution of TOC, total N (TN) and P species, and their relationships to sediment grain size (Kao et al., 2003; Deng et al., 2006; Fang et al., 2007; Zhu et al., 2011a; Meng et al., 2014); several studies have also considered BSi (Liu et al., 2005a; Wang et al., 2014). However, studies on the biogeochemical cycling of TOC, BSi, and various N and P forms in the YRE and adjacent sea, have been largely ignored. To help elucidate the biogeochemical cycling of organic matter and other biogenic elements cycling in the YRE and adjacent sea, we undertook measurements of grain size, TOC, BSi, various N and P fractions, the stable carbon isotope (d13C) and heavy metals in surface sediments. We also investigated factors influencing their distribution, determined the potential bioavailability of N and P, estimated burial fluxes of the biogenic elements, and assessed potential nutrient limitations in these aquatic ecosystems.

http://dx.doi.org/10.1016/j.marpolbul.2015.05.003 0025-326X/Ó 2015 Published by Elsevier Ltd.

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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B. Yang et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx

The YRE is of particular interest to research on organic geochemistry and biogeochemistry because of its global importance (Fig. 1). The Yangtze River is the world’s third longest river (6300 km) and the largest river in China. It has a drainage area of 1.8  106 km2 (Li et al., 2007), annually discharges 9.0  1011 m3 of fresh water, and transports 5.0  108 tons of sediments and 1.2  107 tons of particulate organic matter to the YRE and adjacent sea (Milliman et al., 1985; Chen and Zong, 1998). The hydrodynamic conditions in the study area are very complex, with the main factors including the Changjiang Diluted Water (CDW), the Taiwan Warm Current (TWC), the Kuroshio Current (KC), the Jiangsu Coastal Current (JCC) and the Zhejiang–Fujian Coastal Current (ZFCC) (Fig. 1) (Liu et al., 2007). Generally, a strong northeast winter monsoon prevails from late September to early April, and a weaker southwest summer monsoon occurs from May to August. Most of the Yangtze River-derived sediments are temporarily deposited in the YRE subaqueous delta in the wet season (Liu et al., 2006). During the dry season the stronger northeast monsoon intensifies the coastal currents, the southeastward JCC transports the sediments originally deposited in the old Huanghe delta into the ECS (which may be an important source of sediment to the northern ECS shelf; Hu and Yang, 2001), and the sediments initially deposited in the YRE subaqueous delta are resuspended and transported primarily southward by the ZFCC (Liu et al., 2006). Thus, the largest muddy patch is found in the ECS inner shelf (to approximately 60 m depth), within a narrow band extending from the subaqueous delta southward to the Taiwan Strait. In contrast, because of the absence of a contemporary sediment supply, strong winnowing and resuspension, most of the outer continental shelves of the ECS (water depth 60–200 m) are characterized by relict sand (Wu et al., 2013) that retains the sedimentary characteristics and morphological features of the last stage of the Late Pleistocene (Hu and Yang, 2001). Three field studies were conducted in the YRE and adjacent sea on board the R/V Beidou, in October 2006, and in February and May 2007. The sampling stations are shown in Fig. 1. Surface sediment samples (0–2 cm) from 63 stations were collected using a stainless steel box sampler, and immediately frozen at 20 °C for return to

the laboratory. Prior to analysis the sediment samples were lyophilized, and homogenized by grinding using an agate mortar and pestle. Subsamples were analyzed for biogenic elements, d13C, and heavy metals. Sediment samples taken prior to grinding were used to determine the sediment grain size. Grain size (D, lm) was analyzed using a laser particle size analyzer (Mastersizer 2000; Malvern Instruments Ltd., Malvern, Worcestershire, UK) capable of analyzing particle sizes from 0.02 to 2000 lm. Three sediment size categories were distinguished: (1) clay: D < 4 lm; (2) silt: 4 < D < 63 lm; and (3) sand: D > 63 lm. The samples were analyzed in duplicate, and the analytical relative error was Nfix (30.4%) > Nex (2.8%) (Table 1), suggesting that ON was the main form in the total N pool, and Nfix was the main IN form. Higher concentrations of TN and ON were mainly found in the Zhejiang–Fujian mud area, whereas lower values were recorded for the offshore sites (Fig. 3). The highest values of Nex were found in the Hangzhou Bay mouth, while the highest values of Nfix were found in the offshore region of the Zhejiang–Fujian coast (Fig. 3). The average percentages of the four sedimentary P forms followed the sequence: PDetrital (53.6%) > OP (18.6%) > PCFA (14.5%) > PCDB (13.3%) (Table 1), indicating that IP was the major form in the total P pool, and PDetrital was the most abundant form of IP. The distributions of TP and IP showed a general trend of seaward decrease, and the highest values were found in the north of the YRE. Moreover, the PCDB, PCFA and OP levels exhibited a trend of seaward decrease in the study area (Fig. 3). The PCDB and OP levels showed similar distribution patterns to that of TOC, with the highest values occurring in the mud areas. High concentrations of PCFA were found mainly on the Zhejiang coast, and the highest values were found in the north of the YRE (Fig. 3). The distribution of PDetrital was different from the other IP forms, with low concentrations occurring in the estuarine–ECS inner shelf and increasing values in the ECS outer shelf. The highest values of PDetrital were recorded on the Jiangsu coast (Fig. 3). Sediments from the river mouth to the shelf exhibited d13C values for the bulk organic carbon ranging from 20.7‰ to 23.8‰ (Fig. 4). The most depleted d13C values (12, respectively (Meyers, 1994). The C/P ratio for marine phytoplankton is 106 (Anderson and Sarmiento, 1994), while terrestrial plants can have ratios as high as 800–2050 (van der Zee et al., 2002). In this study both the organic C/N ratio (7–36) and the organic C/P ratio (77–362) were higher than the Redfield ratio (Redfield et al., 1963) (Fig. 4). The strong decreasing trend in the C/N and C/P ratios from the river estuary to the shelf was attributed to a progressive decrease seaward in the deposition of terrestrial organic matter and an increase in marine organic matter inputs. However, the C/N and C/P ratios are of limited use as indicators of sedimentary organic matter, because the original signature of the organic matter may be overprinted or lost by

biochemical alteration prior to and/or soon after deposition (Thornton and McManus, 1994). In general, degradation of ON relative to OC could result in high C/N ratios, which might explain why the highest C/N ratios were found in the offshore region of the Zhejiang–Fujian coast. The high C/P ratios in the offshore area sediments can be explained by preferential P regeneration under oxic decomposition at the sediment–water interface (Epping et al., 2002). Geochemical investigations have usually adopted a two end-member mixing model to quantify the relative proportion of terrestrial organic matter (f%), based on the isotope mass balance (Eq. (2)), as described by Schultz and Calder (1976):

f ð%Þ ¼

d13 Cmarine  d13 Csample d13 Cmarine  d13 Cterrestrial

 100

ð2Þ

where d13Csample is the measured carbon isotope composition. Values of 20‰ (for d13Cmarine) and 26‰ (for d13Cterreserial) were used in this study, based on reported d13C values for marine and terrestrial organic matter (Wu et al., 2003; Zhang et al., 2007). The results revealed that terrestrial organic matter accounted for 12– 63% of the total organic matter in the study area, and showed a trend of decrease from inshore to offshore (Fig. 4), suggesting a

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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B. Yang et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx N 34°

N 34°

33°

33°

32°

0.9

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0.6

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27° 0.2

26°

0.2

26°

TOC 25° 119°

120°

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BSi

126° E

25° 119°

N 34°

N 34°

33°

33°

32°

85

80

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32° 70

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50

70

30° 60

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30 40

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28° 20

30

27°

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26°

10

26° TN

25° 119°

120°

121°

122°

123°

124°

125°

ON

126° E

25° 119°

N 34°

N 34°

33°

33°

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4 3.5

31°

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24 22

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18

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1.5 12

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26° N fix

N ex 25° 119°

120°

121°

122°

123°

124°

125°

126° E

25° 119°

120°

121°

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124°

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126° E

Fig. 3. Distributions of TOC, BSi, N and P concentrations in surface sediments of the YRE and adjacent sea (units: % for TOC and BSi; lmol g1 for the N and P fractions).

progressive seaward increase in the proportion of marine organic matter relative to terrigenous organic matter. In the present study, a large proportion of the terrestrial organic carbon fraction was

found in the mud areas, especially in the YRE and the Zhejiang– Fujian coast (Fig. 4). This is likely to be a consequence of the rapid burial of fluvial carbon, because of enhanced accumulation rates

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

6

B. Yang et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx N 34°

N 34°

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11 12

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9

10

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26° TP

25° 119°

120°

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IP 126° E

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N 34°

33°

33°

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5.5

120°

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2

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26° OP

25° 119°

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PCDB 25° 119°

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N 34°

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PDetrital 120°

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126° E

Fig. 3 (continued)

(Deng et al., 2006) and the refractory nature of fluvial terrestrial organic matter, which is dominated by material derived from soil organic matter (Wu et al., 2007; Hu et al., 2012). This situation is

similar to that described for other large river-dominated marginal seas worldwide, including the coastal margins of the Mississippi River Estuary (Bianchi et al., 2002), the Huanghe (Yellow River)

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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B. Yang et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx Table 1 The concentrations (lmol g1) range (average) and percentage (%) for various forms of sedimentary N and P in surface sediments of the YRE and adjacent sea.

Concentration range Mean concentration Percentage range Average percentage

Concentration range Mean concentration Percentage range Average percentage

Nex

Nfix

IN

ON

TN

0.21–4.06 1.33 0.6–11.1 2.8

8.25–24.62 14.34 16.7–54.1 30.4

8.79–25.70 15.67 18.5–59.2 33.2

8.32–69.12 35.51 40.8–81.5 66.8

18.86–84.77 51.18

PCDB

PCFA

PDetrital

IP

OP

TP

0.78–4.62 2.27 5.4–24.3 13.3

1.36–4.36 2.46 9.1–21.1 14.5

5.09–13.53 8.90 33.5–75.0 53.6

8.36–19.05 13.62 69.6–95.0 81.4

0.76–5.68 3.18 5.0–30.4 18.6

9.70–21.75 16.81

N 34°

N 34°

33°

33° 34

32°

-20.5

32°

32 30

-21

31°

28

31°

26

-21.5

24

30°

30°

22

-22

20

29°

-22.5

29°

18 16

-23

28°

14

28°

12

-23.5

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10

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8

-24

26°

25° 119°

26°

δ 13C 120°

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C/N

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25° 119°

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N 34°

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33° 340

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Terrestrial organic carbon

25° 119°

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126° E

13

Fig. 4. Distributions of d C (‰), the organic C/N and C/P ratios, and the terrestrial organic carbon contribution to TOC (%) in surface sediments of the YRE and adjacent sea.

Estuary (Hu et al., 2009), and the Zhujiang (Pearl River) Estuary (Hu et al., 2006), suggesting that the preservation of terrestrial organic carbon in such coastal margins is a significant process in the global cycle of carbon (Goñi et al., 1998). The highest proportions of marine organic carbon were found near station S0–4 (Fig. 4), which was consistent with this region having the most recent 14C age among surface sediments from the ECS shelf (Wu et al., 2013). Therefore, organic matter in this region is mainly derived from local high levels of primary production (Zhu, 2007).

PCA was performed on the data for TOC, BSi, various N and P fractions, heavy metals, and the sediment grain size. Three principal components (PC1–PC3) distinguished in the analysis accounted for 79% of the total variance (Fig. 5). Principal component 1 (PC1) accounted for 63% of the data variance, and had a high positive loading for the combined variables TOC, TN, ON, OP, PCDB, PCFA, various metals (Al, Fe, Mn, Cr, Cu, Zn, As and Pb), and fine-grained sediments (clay and silt) (Fig. 5), indicating the importance of organic matter in the binding of metal ions to fine-grained sediments.

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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B. Yang et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx

IP

1.0 PDetrital

TP

0.5

PC2 (10%)

BSi Nex

0.0

Sand

Ca

Silt Mn As PCFA Cu PCDB Cr Clay OP Pb Zn TOC Fe Al IN ON TN Nfix

-0.5

-1.0 -1.0

-0.5

0.0

0.5

1.0

PC1 (63%) 1.0

Ca

0.5

BSi

PC3 (6%)

Nfix PCFA PDetrital

IP TP

0.0 Sand Nex

-0.5

TOC IN ON TN Clay Silt Al OP Fe Cr Mn P Zn CDB Cu Pb As

-1.0 -1.0

-0.5

0.0

0.5

1.0

PC1 (63%) Fig. 5. Loading plots for the measured elements and the sediment grain size in the space defined by two components – PC1 versus PC2 and PC3.

These correlations indicated sources associated with terrigenous input, anthropogenic activity and the geochemical matrix. This was based on the allochthonous source of the organic matter measured (Hu et al., 2012) and the high levels of Cr, Cu, Zn, As and Pb associated with anthropogenic sources, including industrial activities and municipal effluents (DelValls et al., 1998; Loska and Wiechuła, 2003; Hudson-Edwards et al., 2004). This was in addition to the Al, Fe and Mn, which are in the geochemical matrix in marine sediments (DelValls et al., 1998; Loska and Wiechuła, 2003). A negative correlation was found between sand and PC1, indicating the absence of organic matter accumulation in this sediment type. Principal component 2 (PC2) accounted for 10% of the total variance, and was characterized by high levels of TP, IP and PDetrital. This component showed that PDetrital was the dominant species of P in surface sediments; PDetrital is mainly attributable to the physical weathering and/or erosion of materials (i.e. magma, igneous and metamorphic rocks) from continents and the strong riverine influence (Ruttenberg, 1992; Ruttenberg and Berner, 1993; Berner and Rao, 1994). For principal component 3 (PC3; 6% of the total variance), high loadings were observed for the concentrations of BSi and Ca in sediments. Based on this association, this component describes the main marine organism composition in the studied sediments (Conley et al., 1993; Bernárdez et al., 2005; Morse et al., 2007). The TOC content showed a general decrease from the estuarine– inner shelf to the outer shelf, which corresponded to the trend of progressive seaward decline in fine-grained sediments (Figs. 2

and 3). Previous studies have shown that fine-grained sediments have a large specific surface area, which provides more binding sites for adsorption of organic matter (Keil et al., 1994; Mayer, 1994); this may help to explain the relatively higher values of TOC in the estuarine–inner shelf mud area compared with the outer shelf region. In addition, the TOC content correlated well with sediment grain size (Table 2), suggesting the influence of hydrodynamic effects on the accumulation of sedimentary organic matter in the study area (Hu et al., 2009, 2012). Consistent with the distribution of TOC, high concentrations of lignin phenols and long-chain (>C20) fatty acids (terrestrial biomarkers) have been recorded in the YRE and on the Zhejiang–Fujian coast; the concentrations gradually decrease seaward from the estuary (Wang et al., 2008; Wu et al., 2013). This observation is consistent with the importance of the Yangtze River as a dominant present-day source of terrestrial TOC to the ECS (Deng et al., 2006; Zhou et al., 2007). The Yangtze River delta (YRD) is an important industrial and economic center for China, but large industrial and municipal discharges are also resulting in high TOC concentrations in the estuarine and coastal regions (Zhou et al., 2007). The BSi in sediments is correlated with the diatom production in the water column (Bernárdez et al., 2005). Increased production of diatoms can lead to an increase in the accumulation of BSi in sediments, which is closely correlated with the primary productivity of adjacent waters (Conley et al., 1993). Previous research showed that the biomass of diatoms offshore from the YRE, and the Zhejiang coastal region was higher than that of the ECS outer shelf (Wu et al., 2000), which may explain, at least in part, the relatively high concentrations of BSi off the YRE and the Zhejiang coast zone compared with the ECS outer shelf. The BSi dissolution rate decreased with increasing fineness of the sediment particles, which is conducive to BSi accumulation (Bernárdez et al., 2006). In this study, the BSi content was highly correlated with clay and silt (Table 2), indicating that sedimentary BSi was apt to accumulate in the fine-grained sediments, resulting in a greater abundance of BSi in the muddy sediments (Figs. 2 and 3). The BSi concentrations were highly correlated with TOC and ON (Table 2), implying that organic matter can reduce the rate of BSi dissolution in sediments (DeMaster, 2002). The high values of TN and ON observed on the Zhejiang–Fujian coast (Fig. 3) may have been caused by anthropogenic activities, such as wastewater discharge and chemical fertilizer use contributing high N levels along the coast (Yan et al., 2010). This speculation is consistent with the high Cr, Cu, Zn, As and Pb concentrations found on the Zhejiang–Fujian coast (Cao et al., 2015); these elements are mainly derived from industrial discharge and fertilizer use (Hudson-Edwards et al., 2004; Mendiguchia et al., 2006; Basaran et al., 2009; Jessop and Turner, 2011). The elevated concentrations of Nex recorded at the Hangzhou Bay mouth (Fig. 3) correspond to the enhanced Cu, Zn, Cr and As concentrations (Cao et al., 2015), and were probably related to inputs of coastal sewage and sediment adsorption (De Lange, 1992; Yan et al., 2010). The high Nfix concentrations observed in the region offshore from the Zhejiang–Fujian coast were probably a result of mineral input from the Yangtze River (Hu et al., 2012), as illite is the main component of clay minerals derived from the Yangtze River (Zhou et al., 2010), and is closely related to Nfix in marine sediments (De Lange, 1992). The concentrations of TP and IP decreased seaward from the estuary because of the huge quantity of particulate P transported by the Yangtze River (Fig. 3; Yu et al., 2012b). The high values of TP and IP in the north of the YRE probably reflect the influence of the abandoned old Huanghe delta by the JCC and input from the Yangtze River (Hu and Yang, 2001; Liu et al., 2007). For instance, Rao and Berner (1997) reported that the concentration of TP in Yangtze River sediments was 19.6 lmol g1.

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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B. Yang et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx Table 2 Correlation analysis results for grain size parameters and the concentrations of biogenic elements in surface sediment.

Clay Silt Sand TOC BSi Nex Nfix ON TN PCDB PCFA PDetrital OP TP a b

Clay

Silt

Sand

TOC

BSi

Nex

Nfix

ON

TN

PCDB

PCFA

PDetrital

OP

0.86a 0.94a 0.82a 0.57a 0.38a 0.64a 0.88a 0.89a 0.77a 0.76a 0.51a 0.71a 0.57a

0.98a 0.74a 0.48a 0.47a 0.59a 0.67a 0.71a 0.78a 0.68a 0.29b 0.62a 0.69a

0.80a 0.53a 0.46a 0.63a 0.77a 0.80a 0.80a 0.73a 0.38a 0.67a 0.67a

0.43a 0.37a 0.67a 0.86a 0.88a 0.75a 0.73a 0.56a 0.64a 0.48a

0.05 0.32b 0.52a 0.53a 0.39a 0.54a 0.12 0.48a 0.53a

0.32b 0.27b 0.33a 0.58a 0.32b 0.27b 0.36a 0.35a

0.62a 0.74a 0.51a 0.53a 0.53a 0.46a 0.23

0.99a 0.73a 0.79a 0.65a 0.76a 0.49a

0.75a 0.79a 0.67a 0.76a 0.47a

0.64a 0.56a 0.71a 0.60a

0.42a 0.60a 0.61a

0.49a 0.16

0.69a

TP

Correlation is significant at the 0.01 level (two-tailed). n = 63. Correlation is significant at the 0.05 level (two-tailed). n = 63.

High concentrations of PCDB and OP were found in the YRE and the Zhejiang–Fujian coastal mud area (Figs. 2 and 3). This elevation of PCDB and OP levels is closely related to anthropogenic activities, and is associated with the input of high concentrations of P from the Yangtze River, and from inputs of coastal domestic sewage and industrial wastewater (Jensen et al., 1995; Ruban et al., 2001; Hou et al., 2009). High concentrations of Cr, Cu, Zn, As and Pb have also been reported in the YRE and the Zhejiang–Fujian coastal mud area (Cao et al., 2015). The fine-grained sediments rich in heavy metals are mainly derived from the Yangtze River (Zhang, 1999; Liu et al., 2006). For instance, unsuccessful management and control of waste drainage into the Yangtze River has resulted in the high heavy metal concentrations in the YRE and adjacent sea. Moreover, the occurrence of heavy metals is significantly correlated with median grain size (p < 0.001) (Cao et al., 2015). This is consistent with the high concentrations of PCDB and OP found in the mud area, derived from fluvial inputs and human activities. However, the spatial variation of OP was not simply a result of physical dilution from the Yangtze River, because the sources were also affected by biological factors (Liu et al., 2004). In addition to anthropogenic inputs, OP is also derived from in situ marine primary productivity (Lukkari et al., 2009), and the Zhejiang–Fujian coast is characterized by high productivity (Zhou et al., 2008). PCFA is mainly derived from the detritus of biological apatite (including bones, teeth, shell fragments), CaCO3-bound P and authigenic carbonate fluorapatite (Sekula-Wood et al., 2012). The Zhejiang coast is an important fishery and mariculture area in China, and relatively high concentrations of Ca have been reported from the north of the YRE (Cao et al., 2015), where the carbonate content in sediments is high and has resulted in much calcium carbonate deposition (Yu et al., 2013). Thus, the high PCFA concentrations on the Zhejiang coast were likely to have originated from the detritus of marine organisms (Zhuang et al., 2014), and the concentrations of CaCO3-bound P are expected to be higher in the north of the YRE (Liu et al., 2004). PDetrital is closely associated with the coarser fractions of sediment, and represents coarser-grained inert material derived from the erosion of magma, and igneous and metamorphic rocks (Ruttenberg, 1992; Berner and Rao, 1994). In this study, the concentrations of PDetrital in the estuarine–inner ECS shelf were low, but increased toward the outer shelf (Fig. 3). This is probably related to the presence of relict sand deposited in the Late Pleistocene from the Yangtze and Huanghe Rivers (Hu and Yang, 2001). However, the highest values of PDetrital were observed on the Jiangsu coast, where the percentages of clay and silt accounted for an average of 70% of total sediments (Figs. 2 and 3). This is

probably associated with the transport of old Huanghe delta sediments. In drainage basins the PDetrital is primarily of terrestrial origin, derived from the weathering of rocks (Ruttenberg, 1992). Compared with the Yangtze River sediments, the Huanghe River sediments are characterized by high apatite concentrations (Yang et al., 2004). Thus, the delivery of old Huanghe delta sediment rich in apatite may partly explain the high concentrations of PDetrital on the Jiangsu coast (Yu et al., 2013). Furthermore, the PCDB, OP, PCFA and N fractions were highly correlated with the clay, silt and TOC content (Table 2), suggesting that grain size may be a significant factor controlling the concentrations and distribution of PCDB, OP, PCFA and N, as well as the abundant accumulation of these fractions in the fine-grained organic-rich sediments. Distinguishing N and P speciation is essential for understanding the upper limit of the potential bioavailability of these elements in aquatic ecosystems. Only certain species of N and P can be transformed in sediments into bioavailable forms, through physical, chemical and biological processes. If N and P release from the sediment occurs, primary productivity can increase markedly in the overlying water, and even in the upper water column (Tyler et al., 2003; Coelho et al., 2004). As noted previously, Nex is the most active fraction of N in sediments, and can be directly released from the sediment (De Lange, 1992). Nfix (also known as non-exchangeable ammonium) is present in the mineral crystal lattice, and is considered to be insoluble and non-reactive in marine sediments, while ON can become bioavailable through microorganism decomposition (Hedges and Oades, 1997). Therefore, Nex and ON should be considered to be potentially bioavailable N in aquatic ecosystems, and their combined total represents the upper limit of N that can be released into overlying water. Consequently, 0.6–81.5% (average, 79.6%) of the TN in the YRE and adjacent sea is potentially bioavailable, representing a large proportion of the sedimentary N pool. PCDB consists of loosely sorbed P and Fe-bound P, which can be released from sediments into the overlying water through physical–chemical factors including the hydrodynamic conditions, bioturbation and redox changes (Andrieux and Aminot, 1997; Coelho et al., 2004; Chen et al., 2011). PCFA and PDetrital are considered to comprise the refractory fraction of sedimentary P and a permanent sink of reactive P in marine sediments (Ruttenberg and Berner, 1993; Andrieux and Aminot, 1997; van der Zee et al., 2002). OP is more available for biological use following remineralization and microbial decomposition (Andrieux and Aminot, 1997; Sutula et al., 2004). Therefore, PCDB and OP are potentially bioavailable P, and their combined total represents the upper limit of P that can be released into overlying water

Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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(Andrieux and Aminot, 1997; Zhuang et al., 2014). Consequently, the concentration of bioavailable P in surface sediments of the YRE and adjacent sea was 1.99–9.72 lmol g1, which accounts for 13.5–52.1% of TP (average, 31.8%); thus, bioavailable P accounted for a substantial proportion of the sedimentary P pool. Knowledge of the burial fluxes of biogenic elements is required for understanding how many biogenic elements become buried in sediments. The burial fluxes (BF) of TOC, BSi, TN and TP (lmol cm2 yr1) were calculated using Eq. (3) (Ingall and Jahnke, 1994):

BF ¼ C i x ¼ C i Sð1  uÞqs

ð3Þ

1

where Ci (lmol g ) is the concentration of biogenic elements in surface sediments; x (g cm2 yr1) is the sediment mass accumulation rate; S (cm yr1) is the sedimentation rate; u is the average sediment porosity; and qs (g cm3) is the density of sediment solids (qs in the present study was 2.1 g cm3; Song et al., 2014). The data for the sedimentation rate were derived from published reports (Huh and Su, 1999; Su and Huh, 2002; Liu et al., 2006; Li et al., 2012). In the present study, the burial fluxes for TOC, BSi, TN and TP were 39.74–2194.32, 17.34–517.48, 5.02–188.85 and 3.10– 62.72 lmol cm2 yr1, respectively (Fig. 6). The burial fluxes of

TOC and TN in the study area were higher than those reported for TOC in the Mediterranean Sea (25–975 lmol cm2 yr1; Giordani et al., 2002) and TN in the southern Yellow Sea (2.77– 16.83 lmol cm2 yr1; Lü et al., 2005). This discrepancy is probably because the study area is characterized by a high sediment deposition rate, and high levels of terrestrial input and primary productivity (Deng et al., 2006; Li et al., 2011). The burial fluxes for BSi were within the range reported by Liu et al. (2005a) for the ECS, and the TP burial fluxes were within the values previously reported for the Bohai and Yellow Seas, and the middle shelf of the ECS (Liu et al., 2004; Fang et al., 2007). The maximum burial fluxes for TOC, BSi, TN and TP occurred in the YRE (Fig. 6), where the highest sedimentation rate reached up to 6 cm yr1 (Li et al., 2012). The sedimentation rate was positively correlated with the burial fluxes for TOC (r = 0.87, p < 0.01), BSi (r = 0.90, p < 0.01), TN (r = 0.95, p < 0.01) and TP (r = 0.94, p < 0.01), respectively, indicating that the sedimentation rate was a dominant factor affecting the burial fluxes for biogenic elements. Moreover, our results show that there was a significant relationship between the burial flux for TN and sediment porosity in the study area (r = 0.31, p < 0.05), suggesting that sediment porosity is probably a significant factor affecting the TN burial flux. Other environmental factors including the bioturbation rate, microbial

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Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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activity and bottom water oxygen conditions will also affect the burial fluxes of biogenic elements in marine sediments (Schenau et al., 2005), but assessment of the influencing of other factors on burial flux is required to more comprehensively understand this processes. With the rapid increase in recent decades in development of the economy of the Yangtze River basin, abundant nutrients have been delivered into the Yangtze River (Zhou et al., 2008). Changes in riverine nutrient concentrations and their ratios may influence estuarine and coastal ecosystems (Liu et al., 2003a). Based on monitoring data from Datong station (625 km upstream of the YRE mouth), N and P inputs to the YRE and adjacent sea have sharply increased since the 1960s, mainly because of chemical fertilizer use in the Yangtze River catchment (Yu et al., 2012a). The concentration of nitrate in the estuary has increased by almost a factor of three, and the dissolved P concentration has increased by nearly 30% in the last four decades (Zhou et al., 2008). Excessive inputs of anthropogenic nutrients have been resulted in the frequent occurrence of harmful algal blooms in the YRE and adjacent sea since the 1980s (Zhou et al., 2003). Moreover, dissolved silicate in the Yangtze River began to decrease after the 1960s, as a result of the construction of reservoirs and dams along the river, and the decrease accelerated after the 1980s (Li et al., 2007). Increasing N/P and N/Si ratios may be expected to exercise a significant influence on the ecological system of the YRE and adjacent sea. For example, as a consequence of the increased of N/P ratio and the decreased of Si/N ratio following impoundment (June 2003) of the Yangtze River by the Three Gorges Dam (TGD), the entire study area may be subject to serious P and Si limitation following closure of the TGD (Chai et al., 2009). This is because marine phytoplankton consume the P and Si in overlying water, and it is then transported to depth by the biological pump, and ultimately deposited in the sediments; this is highlighted by the burial fluxes of TP and BSi determined in the present study, which showed fluxes up to 62.72 and 517.48 lmol cm2 yr1 (Fig. 6), respectively. The mean (range) molar ratios of total N/P and Si/P were 3.0 (1.2–5.0) and 8.8 (5.0–14.8), respectively, suggesting that the P is likely to be deposited in surface sediments. The Si/N ratio was 3.2 (1.2–6.8), indicating that Si is also probably to be deposited in sediments. The OC/Si, ON/Si and OP/Si ratios in surface sediments were 2.92 (1.47–6.13), 0.24 (0.06–0.53) and 0.02 (0.01– 0.05), respectively. The mean molar ratios of OC/Si, ON/Si and OP/Si in fresh marine planktonic organic matter are approximately 6.63, 1.00 and 0.06, respectively (Redfield et al., 1963). The Redfield ratios of OC/Si, ON/Si and OP/Si are higher than the ratios in the present study, suggesting that the organic matter arriving at the

surface sediments was not fresh marine detritus; the decomposition rate of organic matter was higher than that of the BSi dissolution rate in the same submarine environment. Regression analysis showed that the PCDB and TP concentrations were positively correlated with the total Fe content (Fig. 7), consistent with previous findings for coastal areas (Moutin et al., 1993; Andrieux-Loyer and Aminot, 2001). The significant linear relationship between PCDB and Fe (Fig. 7a) may partly be attributed to the adsorption of phosphate on iron oxides (Wang et al., 2009). As shown in Fig. 7a, a significant X-axis intercept (12.86 g kg1) is thought to indicate the presence of Fe-rich mineral phases, and a relatively low phosphate surface interaction or a relatively low occluded phosphate concentration (Andrieux-Loyer and Aminot, 2001). However, the large Y-axis intercept (366.45 mg kg1) in Fig. 7b suggests the occurrence of P in non-Fe mineral phases. Gerritse et al. (1998) found that for virgin sediments of the Swan-canning estuary, Western Australia, the TP and total Fe had a significant linear relationship: TP (mg kg1) = 7Fe (g kg1) + 20. The extraordinarily small intercept (20 mg kg1) indicated extremely low levels of P in the non-Fe mineral phases for the virgin sediment. The molar ratio of total Fe to TP was 21–61 in the YRE and adjacent sea. The ratios for sediments from the Daliao River system (China) and from the French coastal region were 16–34 and 7–14, respectively (Andrieux-Loyer and Aminot, 2001; Wang et al., 2009). It has previously been reported that freshwater sediments having a total Fe/P molar ratio >8.5 are capable of retaining phosphate in the oxidizing surface layer, but that phosphate leached when the ratio was Nfix (30.4%) > Nex (2.8%). PDetrital was the dominant P-bearing component (53.6%), followed by OP (18.6%), PCFA (14.5%) and PCDB (13.3%). Bioavailable N potentially represented 79.6% (0.6–81.5%) of TN, and comprised a great proportion of the

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Please cite this article in press as: Yang, B., et al. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River Estuary and adjacent sea. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.003

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sedimentary N pool. Bioavailable P potentially accounted for 31.8% (13.5–52.1%) of TP, and accounted for a substantial proportion of the sedimentary P pool. The burial fluxes for TOC, BSi, TN and TP were dominated by the sedimentation rate. The molar ratios of total N/P (1.2–5.0) and Si/P (5.0–14.8) suggested that the P is likely to be deposited in the sediments, and the total Fe/P molar ratio (21–61) suggested that the iron oxides/hydroxides in surface sediments may be able to sequester more P, which could potentially result in more serious P limitation for the growth of phytoplankton in the submarine ecosystem involved. Acknowledgements We wish to thank the captain and crews of the R/V Beidou for their help and cooperation during the study. We are also sincerely grateful to colleagues from the marine biogeochemistry laboratory for their help in field sampling. We acknowledge the SKLEC, East China Normal University for assistance with grain size, TOC, TN and d13C analyses, and we are grateful to Dr. K.Y. Choi for help with heavy metal analyses in the KIOST. This work was supported by grants for the National Natural Science Foundation of China (Nos. 40925017 and 41221004), the National Basic Research Program of China (No. 2011CB409802). This study is a contribution to the international IMBER project. References Anderson, L.D., Delaney, M.L., 2000. Sequential extraction and analysis of phosphorus in marine sediments: streamlining of the SEDEX procedure. Limnol. Oceanogr. 45, 509–515. Anderson, L.A., Sarmiento, J.L., 1994. Redfield ratios of remineralization determined by nutrient data analysis. Global Biogeochem. Cycles 8, 65–80. Andrieux, F., Aminot, A., 1997. A two-year survey of phosphorus speciation in the sediments of the Bay of Seine (France). Cont. Shelf Res. 17, 1229–1245. Andrieux-Loyer, F., Aminot, A., 2001. Phosphorus forms related to sediment grain size and geochemical characteristics in French coastal areas. Estuarine, Cont. Shelf Res. 52, 617–629. Aspila, K.I., Agemian, H., Chau, A.S.Y., 1976. A semi-automated method for the determination of inorganic, organic and total phosphate in sediments. Analyst 101, 187–197. Basaran, A.K., Aksu, M., Egemen, O., 2009. Impacts of the fish farms on the water column nutrient concentrations and accumulation of heavy metals in the sediments in the eastern Aegean Sea (Turkey). Environ. Monit. Assess. 162, 439– 451. Bernárdez, P., Prego, R., Francés, G., González-Alvarez, R., 2005. Opal content in the Ría de Vigo and Galician continental shelf: biogenic silica in the muddy fraction as an accurate paleoproductivity proxy. Cont. Shelf Res. 25, 1249–1264. Bernárdez, P., Francés, G., Prego, R., 2006. Benthic–pelagic coupling and postdepositional processes as revealed by the distribution of opal in sediments: the case of the Ría de Vigo (NW Iberian Peninsula). Estuar. Coast. Shelf Sci. 68, 271–281. Berner, R.A., Rao, J.L., 1994. Phosphorus in sediments of the Amazon River and estuary: implications for the global flux of phosphorus to the sea. Geochim. Cosmochim. Acta 58, 2333–2339. Bianchi, T.S., Allison, M.A., 2009. Large-river delta-front estuaries as natural ‘‘recorders’’ of global environmental change. Proc. Natl. Acad. Sci. 106, 8085– 8092. Bianchi, T.S., Mitra, S., McKee, B.A., 2002. Sources of terrestrially-derived organic carbon in lower Mississippi River and Louisiana shelf sediments: implications for differential sedimentation and transport at the coastal margin. Mar. Chem. 77, 211–223. Cao, L., Hong, G.H., Liu, S.M., 2015. Metal elements in the bottom sediments of the Changjiang Estuary and its adjacent continental shelf of the East China Sea. Mar. Pollut. Bull. http://dx.doi.org/10.1016/j.marpolbul.2015.03.013. Chai, C., Yu, Z.M., Song, X.X., Cao, X.H., 2006. The status and characteristics of eutrophication in the Yangtze River (Changjiang) estuary and the adjacent East China Sea, China. Hydrobiologia 563, 313–328. Chai, C., Yu, Z.M., Shen, Z.L., Song, X.X., Cao, X.H., Yao, Y., 2009. Nutrient characteristics in the Yangtze River Estuary and the adjacent East China Sea before and after impoundment of the Three Gorges Dam. Sci. Total Environ. 407, 4687–4695. Chen, X., Zong, Y., 1998. Coastal erosion along the Changjiang deltaic shoreline, China: history and prospective. Estuar. Coast. Shelf Sci. 46, 733–742. Chen, J.J., Lu, S.Y., Zhao, Y.K., Wang, W., Huang, M.S., 2011. Effects of overlying water aeration on phosphorus fractions and alkaline phosphatase activity in surface sediment. J. Environ. Sci. 23, 206–211. Cifuentes, L.A., Eldridge, P.M., 1998. A mass and isotope balance model of DOC mixing in estuaries. Limnol. Oceanogr. 43, 1872–1882.

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