Organic matter degradation in surface sediments of

Science of the Total Environment 637–638 (2018) 1004–1013

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Organic matter degradation in surface sediments of the Changjiang estuary: Evidence from amino acids Kui Wang a, Jianfang Chen a,⁎, Haiyan Jin a, Hongliang Li a, Weiyan Zhang b a b

Key Lab of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China Key Lab of Submarine Geosciences, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• An amino acids–based degradation index (DI) was mapped across the Changjiang Estuary. • Sediments with more terrestrial material were generally more refractory. • Organic matter was freshest in marinesourced and silt-clay hypoxic sediments. • DI was 39% associated with source material and bottom water oxygen combined.

a r t i c l e

i n f o

Article history: Received 12 February 2018 Received in revised form 16 April 2018 Accepted 17 April 2018 Available online xxxx Editor: Jay Gan Keywords: Amino acid Degradation Sediment

a b s t r a c t Organic matter degradation is a key component of the processes of carbon preservation and burial in seafloor sediments. The aim of this study was to explore organic matter degradation state within the open-shelf Changjiang Estuary of the East China Sea, using an amino acids–based degradation index (DI) in conjunction with information about organic matter source (marine versus terrestrial), bottom water oxygenation state, and sediment grain size. The relative molar percentages of 17 individual amino acids (characterized using principal component analysis) in surface sediments indicate that organic matter is degraded to varying extents across the estuary seabed. Sediments with DI N0 (relatively labile) were found mostly within a coastal hypoxic area. Sediments of DI less than −1 (relatively refractory) were found near the Changjiang River mouth and the northern and southern parts of the central shelf. We consider DI to be a more reliable indicator of degradation than simple ratios of AAs. DI was inversely correlated with the proportion of terrestrial organic material (Ft) in the sediments, indicating that relatively fresh/labile organic matter was generally associated with marine sources. DI was significantly correlated with Ft and bottom water apparent oxygen utilization (AOUbot) together. The parameter DI and the (labile) amino acid tyrosine were highest in hypoxic areas, suggesting the presence of relatively fresh organic matter, probably due to a combination of marine-source inputs and better preservation of organic matter in the silt and clay sediments of these areas (as compared to sandy sediments). Less degraded organic matter with high amino acids was also favorable to benthic animals. Overall, sedimentary estuarine organic matter was least degraded in areas characterized by marine sources of organic matter, low-oxygen conditions, and fine-grained sediments. © 2018 Elsevier B.V. All rights reserved.

⁎ Corresponding author. E-mail addresses: [email protected] (K. Wang), [email protected] (J. Chen), [email protected] (H. Jin), [email protected] (H. Li).

https://doi.org/10.1016/j.scitotenv.2018.04.242 0048-9697/© 2018 Elsevier B.V. All rights reserved.

K. Wang et al. / Science of the Total Environment 637–638 (2018) 1004–1013

1. Introduction Marine surface sediments constitute an important carbon burial interface, where large amounts of organic carbon (OC) produced in upper waters are received, degraded (mostly by microorganisms) (Jørgensen, 2000), and finally buried. The consumption of oxygen in the course of organic matter degradation may strengthen hypoxia (Zhang et al., 2010), consequently amplifying ocean acidification (Hauri et al., 2009; Cai, 2011; Melzner et al., 2013) and accelerating the release of CO2 to the atmosphere. On the shallower continental shelves, however, the factors influencing OM degradation are more complex. Fresh autochthonous estuarine organic matter mixing with highly degraded allocthonous terrestrial organic matter (Raymond and Bauer, 2001), strong horizontal oxygen gradients in estuaries (Hulthe et al., 1998; Vandewiele et al., 2009) and sediment grain size (Mayer, 1994), all these factors will affect the OM degradation states prominently. Understanding estuarine OM preservation and burial and its relation to carbon cycling requires the identification of differences in OM degradation state as well as the main factors or processes affecting OM in surface sediments. Amino acids (AAs) are useful indicators of degradation in the marine environment (Cowie and Hedges, 1992; Dauwe et al., 1999; Lee et al., 2000).For example, intracellular amino acids present in cell plasma (glutamic acid, tyrosine, phenylalanine, and methionine) (Hecky et al., 1973) are more susceptible to degradation than are cell wall– associated amino acids (glycine, serine, alanine, and oysine). Similarly, the mole percentages of some non-protein amino acids, (e.g., βalanine + γ-aminobutyric acid, β-Ala + γ-Aba) are elevated in sedimentary mixtures exposed to oxic degradation, because non-protein AAs are much less reactive than protein AAs. (Cowie and Hedges, 1992; Cowie et al., 1992; Dauwe and Middelburg, 1998; Suthhof et al., 2000). The Changjiang Estuary of the East China Sea is a typical large river– dominated estuary, globally prominent among continental shelf ecosystems. Across the Changjiang Estuary shelf, fresh, labile (autochthonous) marine organic matter is mixed with degraded and refractory terrestrial organic matter to varying extents. Meanwhile, strong summer stratification of the water column in conjunction with the sinking and respiration of biogenic particles frequently results in hypoxic events (Li et al., 2002; Wei et al., 2007; Zhou et al., 2009; Qian et al., 2016). These variability in OM source and oxygen conditions would be expected to influence the bulk degradation state of the surface sediments. Previous studies in the region have used particulate and dissolved AAs to investigate the degradation of suspended particulate matter (Wu et al., 2007a; Zhu et al., 2014). Still, local controls on OM degradation state in the sediments (e.g., different OM sources or bottom-water oxygen conditions) remain unclear, as do their interrelationships. In this study, we used amino acid pool compositions to quantify OM degradation state in the sediments of the Changjiang Estuary and established correlations of degradation state with marine versus terrestrial source contributions and bottom water oxygen utilization. We also compared different AA-based methods of quantifying organic matter degradation state or lability. The overarching aim was to provide a better understanding of sedimentary source and oxygen gradient controls on OM degradation in estuarine sediments. 2. Material and methods 2.1. Study area The Changjiang Estuary (Fig. 1) is one of the world's most productive continental shelf areas. Annually, the Changjiang River (Yangtze River) delivers to the estuary a large sediment load of approximately 4.8 × 108 t (Milliman and Meade, 1983) and a freshwater discharge of approximately 14.8 × 107 m3 (Dai et al., 2014). Mixing of this eutrophic fresh water with the oligotrophic water of the Kuroshio Current gives

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rise to strong cross-shelf gradients of salinity and nutrients (Zhang et al., 2007a). Marine biogenic particles resulting from surface-water primary production settle toward the seafloor, especially in the vicinity of the river plume, and are respired in the water column and surface sediments, resulting in oxygen consumption and frequent seasonal hypoxia (Li et al., 2002; Wei et al., 2007; Zhu et al., 2011; Zhu et al., 2016). The season for hypoxia events usually begins in early June and may persist as late as October (Zhu et al., 2016; Zhou et al., 2017). 2.2. Sampling methods Samples of surface sediments (0–2 cm depth; n = 149) were collected at 149 stations during a research cruise in the Changjiang Estuary, 4 April to 17 May 2007 (Fig. 1). A steel grab sampler was used to recover the sediments, which were subsampled on deck and then frozen at −20 °C for later analysis. Samples of suspended particulate matter (n = 18) were collected at 4 stations during 1–17 June 2009 (Fig. 1). Each sample of 500–2000 ml seawater was passed through a 47 mm diameter GF/F filter (pore size of 0.7 μm) before being stored at −20 °C for later analysis. For chlorophyll a (Chl a) analyses, each sample of 100–250 ml seawater was passed through a GF/F filter, which was then stored at −20 °C for later processing. Bottom waters (sampled at a height of 2 m above the seabed) were collected at 149 stations during 15 July to 10 September 2006 (Fig. 1). Seawater was collected into Niskin bottles attached to a CTD rosette, and the samples (n = 149) were later analyzed for dissolved oxygen content. The three sample sets were collected during different time periods, but we consider them to be generally representative of typical summer conditions in our study area. In recent decades, summer hypoxia has typically occurred in the same general areas (Zhu et al., 2011). In addition, surface sediment geochemistry exhibits little seasonal variability due to low sedimentation rates in most parts of the estuary (Liu et al., 2006). 2.3. Sediment analyses: AAs, OC, TN, δ13C, Ft, and grain size To quantify sedimentary total hydrolyzable amino acids (THAAs; n = 47) and HAs (n = 47), we dried and ground sediment subsamples before washing them with Milli-Q® water in a supersonic box for desalting. Aqueous hydrolyses were conducted in 6 N HCl under N2 gas for 24 h at 110 °C. The hydrolysis mixture was dried and then dissolved in Milli-Q® water; the component amino acids were derived according to the Waters® AccQ·Tag™ method (Cohen and Michaud, 1993). The derivatives were determined with a Waters® 600E pump system (multisolvent delivery system) and a Waters® 474 fluorescence detector; the THAA and HA data were processed with a Waters® Millennium®32 chromatography station. Results from duplicate samples of individual AAs showed the coefficient of variation to be b5.6%; for THAA, the coefficient of variation was 2.1%. The external AA and HA standard solution (Sigma-Aldrich®) contained 17 individual amino acids: alanine (Ala), arginine (Arg), aspartic acid (Asp), cystine (Cys), glutamic acid (Glu), glycine (Gly), histidine (His), isoleucine (Iso), leucine (Leu), lysine (Lys), methionine (Met), phenylalanine (Phe), proline (Pro), serine (Ser), threonine (Thr), tyrosine (Tyr), and valine (Val). To this solution, the hexosamine standards galactosamine (Gal) and glucosamine (Gluco) were added, as were two non-protein amino acids, β-alanine (β-Ala) and γ-amino butyric acid (γ-Aba). The internal standard α-amino butyric acid (α-Aba) was also added for the determination of recovery rate, which was calculated to be between 92.1% and 103.7%. After inorganic carbon was removed from the sediment samples (using 1 N HCl), concentrations of organic carbon (n = 149) and total nitrogen (n = 149) and ratios of stable carbon isotopes (n = 149) were determined with an isotope ratio mass spectrometer (Delta Plus

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Fig. 1. Map of the Changjiang River estuary. The Changjiang River enters the East China Sea north of Shanghai; Hangzhou Bay is the large estuary south of Shanghai. The archipelago islands in the southwest corner are the Zhoushan Islands. Dots indicate stations where surface sediments and bottom-water samples were collected, and triangles indicate stations where suspended particles were sampled. Each inner-shelf transect is labeled at its westernmost station. The colors indicate water depth. The white arrows show predominant currents.

AD EA-IRMS, Thermal Finnigan Incorporation); the average error was b0.2‰. Isotopic results are given in the conventional δ notation:

Bottom water dissolved oxygen (DO) was measured using the Winkler titration method (Grasshoff et al., 1999).

δ13 C ¼ Rsample =Rstandard −1 1000‰

2.5. Data analyses

ð1Þ

where R refers to the 13C/12C ratios of the sample and the reference (standard) gas. Isotopic data are based on the international Vienna Pee Dee Belemnite (PDB) standard. The fraction of terrestrial organic matter, Ft, in a sample is given by: F t ¼ δ13 Cm −δ13 Ct = δ13 Cm −δ13 Cs 100%

ð2Þ

where δ13Cm and δ13Ct are the δ13C values of marine and terrestrial endmembers, and δ13Cs is the δ13C value of the sediment sample. The central assumption is that the sample OM is composed exclusively of terrestrial OM delivered by the Changjiang River (δ13C = −25.6‰) (Wu et al., 2007b; Xing et al., 2011) and marine OM derived from local sources (δ13C = −20.0‰) (Zhang et al., 2007b; Xing et al., 2011). The fraction of marine organic matter, Fm, is given by as Fm = 1 − Ft. Carbon in THAA and HA, expressed as a percentage of organic carbon (AA-C%OC and HA-C%OC), was calculated based on individual amino acid mass weights. Nitrogen in THAA and HA, expressed as a percentage of total nitrogen (AA-N%TN and HA-N%TN), was similarly calculated. Grain size analyses were conducted using an H2250 Laser Diffraction HelosSystem (Sympatec, Clausthal-Zellerfeld, Germany). For analyses of THAA, HA, and δ13C in suspended particulate matter, samples were collected onto a GF/F membrane and then analyzed according to the same protocol as the surface sediment samples. 2.4. Seawater analyses: Chl a and bottom water DO The Chl a samples were extracted with 10 ml 90% acetone at −20 °C. Concentrations were determined with a Turner Designs 10-AU fluorometer according to the fluorometric acidification procedure of (HolmHansen et al., 1965).

To quantify differences in organic matter quality and degradation state, a principal component analysis (PCA) was carried out using the relative molar percentages (mol%) of individual amino acids from samples of surface sediments and suspended particulate matter. The first component, namely the site score or degradation index developed by Dauwe and Middelburg (1998) and Dauwe et al. (1999), was calculated using: DI ¼ Σi ½ð vari −AVR vari Þ=STD vari fac:coef:i

ð3Þ

where vari is the mole percent of amino acid i, AVG vari and STD vari are the mean and standard deviation, and fac.coef.i is the factor score coefficient. Higher values of DI indicate greater lability. Organic matter with DI b 0.5 is considered to be extensively degraded (Dauwe et al., 1999). In earlier work examining the use of amino acids and hexosamines as indicators of organic matter degradation state in surface sediments (Dauwe and Middelburg, 1998), the first component of a comprehensive principal component analysis was taken as a degradation index that indicated the status of organic matter from different source materials. The higher the DI (Eq. (3)), the greater lability the organic matter (Dauwe and Middelburg, 1998). For our Changjiang Estuary samples, we similarly derived values of DI (Eq. (2)) from the molar percentages of individual amino acids in seafloor sediments at 47 locations across the estuary and in suspended particulate matter at 4 mid-shelf stations. All correlation analyses performed in this study use Pearson's correlation coefficients: p b 0.05 indicates a statistically significant correlation (or the correlation is significant at the α = 0.05 level, 2-tailed), whereas p b 0.01 indicates a highly significant correlation (as the correlation is significant at the α = 0.01 level, 2-tailed). Significant differences between two sets of samples were tested for using a t-test at α = 0.05.


SPSS® software (version 13.0) was used to perform simple and multiple regressions. All maps were created using the free Ocean Data View software, version 4.6.4 (Schlitzer, 2016). 3. Results 3.1. Surface sediment organic matter: elemental and isotopic compositions Organic carbon (Fig. 2a) and total nitrogen (Fig. 2b) in surface sediments exhibited similar distributions. Generally, these constituents were relatively high at the Changjiang River mouth and in Hangzhou Bay. Belts of lower values ran southeast/northwest across the middle of the estuary. In the nearshore zone, the highest OC value was 1.27%, at station M4–5 (on the inner shelf due east of Shanghai). The lowest OC overall (0.01%) occurred at stations M2–5 and M2–6. The highest nearshore TN was 0.103%, at station O7–1. The lowest TN overall (0.015%) occurred at stations M1–12 and M2–10. Values of δ13C (Fig. 2c;) in surface sediments ranged from −24.98‰ to −20.35‰, with an overall average of −22.08‰. Lowest values generally occurred along the coast, including the areas of the Changjiang River mouth and Hangzhou Bay. Values of δ13C increased significantly with increasing water depth (r = 0.69, p b 0.001, n = 108), with decreasing OC (r = −0.507, p b 0.001, n = 108), and with decreasing TN (r = −0.229, p b 0.0173, n = 108). Relatively high values of δ13C occurred in the central part of the research area, in a southeast/northwest– trending band. The most positive (i.e., least negative) δ13C value (−20.35‰) occurred at station M1–8. The nearshore stations had low negative values, with the most negative value (−24.98‰) occurring at station M4–5. Values of organic carbon/total nitrogen (Corganic/Ntotal, molar ratio) ranged from 0.7 (station M2–6, just seaward of the Changjiang river mouth) to 32.8 (station M5–5, in the Changjiang river channel), with an overall average of 12.9 (Fig. 2d). Corganic/Ntotal values were generally highest in the vicinity of the Changjiang river mouth. An area of high Corganic/Ntotal was also encountered in the mid-shelf area east of the river mouth. 3.2. Surface sediments: THAA, HA, individual AAs, and DI Sedimentary concentrations of total hydrolyzable amino acids (Fig. 3a) and hexosamines (Fig. 3b) were highly variable. THAA was high just off Hangzhou Bay, between 122°E and 123°E (highest at

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station O7–4, at 2.38 mg g−1), and eastward of 125°E (highest at station C14–6, at 2.30 mg g−1). Lower values were encountered in the northcentral area between 123.5°E and 125°E (e.g., 0.33 mg g−1 at stations L2–11 and M2–10); the lowest value (0.20 mg g−1) occurred at station M3–1, seaward of the Changjiang river mouth. The HA distribution was similar to that of THAA. Among individual amino acids, Gly exhibited the generally highest molar percentages (between 10% and 20%), followed by (in descending order within the range of about 5% to 10%) Ala, Asp, Cys, Val, Glu, and Thr. The amino acids Pro, Leu, Ser, Arg, Ile, Met, Phe, and Lys were at all present in relatively low molar percentages (b5% on average); His and Tyr were the lowest (mostly under 1%). The non-protein amino acids β-Ala and γ-Aba were high in nearshore and offshore areas (e.g., 2.41% β-Ala at station C14–3 and 3.5% γ-Aba at station C20–3) but very low in the north-central part of the study area (at times lower even than the detection limit). The DI values of the surface sediments were mostly b0.50 (Fig. 4a) — e.g., in the Changjiang River channel and in the north- and south-central estuary. The lowest DI (least labile) was −8.17, at Changjiang River station M5–7. Surface sediments with DI N 0.50 were encountered at nearshore stations M1–1, M1–3, M3–3, and M4–1; at mid-shelf station M4–11 (west of 123°E); and at offshore station C14–6 (seaward of 126°E) (Fig. 4a). The highest DI (most labile) was 2.40, at mid-shelf station M4–11. 3.3. Surface sediments: carbon and nitrogen in THAA and HA, Glu/γ-Aba and Asp/β-Ala molar ratios Carbon and nitrogen in amino acids accounted for a large fraction of the OC and TN in surface sediments (Supplemental Table 1). Areas of high AA-C%OC (Fig. 3c) and AA-N%TN (Fig. 3d) occurred in the north-central and south-central parts of the study area. Values of AA-C%OC ranged up to 40.6% (station M1–7), while AA-N%TN ranged up to 43.0% (station N5–4). The more nearshore and offshore areas exhibited lower AA-C%OC (minimum value = 3.0%, at nearshore station M3–1) and AA-N%TN (minimum value = 6.4%, at midshelf station M4–13). Carbon and nitrogen in hexosamines accounted for a very minor fraction of sedimentary OC and TN (Supplemental Table 1). Values of HA-C%OC (Fig. 3e) ranged between 0.3% (nearshore station M3–1) and 6.5% (river-plume station M1–7). Values of HA-N%TN (Fig. 3f) ranged between 0.1% (river channel station M5–7) and 6.7% (mid-

Fig. 2. Distributions of bulk surface sediment properties in the Changjiang Estuary: (a) organic carbon, (b) total nitrogen, (c) δ13C, and (d) organic carbon/total nitrogen ratio.

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Fig. 3. Distributions of amino acid–associated properties in surface sediments of the Changjiang Estuary: (a) total hydrolyzable amino acids, (b) hexosamines, (c) THAA-associated organic carbon, as a percentage of OC, (d) THAA-associated nitrogen, as a percentage of TN, (e) HA-associated organic carbon, as a percentage of OC, and (f) HA-associated nitrogen, as a percentage of TN.

shelf station M4–11). In the surface sediments, the Glu/γ-Aba ratio (Fig. 4b) and the Asp/β-Ala ratio (Fig. 4c) were both very high in the north-central area (with maximum values of 5.21 and 10.71,

respectively, at station M2–12) due to the low molar percentages of the end products γ-Aba and β-Ala. In this area, (e.g., station M2–10), β-Ala was below the detection limit.

Fig. 4. Distributions of degradation-related surface sediment properties: (a) degradation index, (b) Glu/γ-Aba, (c) Asp/β-Ala, and (d) fraction of terrestrial organic matter, Ft.


3.4. Suspended particulates: DI, Chl a, and δ13C, Glu/γ-Aba and Asp/β-Ala molar ratios The DI values of suspended particulate matter at the 4 profile stations (Fig. 5a) were all N1 (i.e., relatively labile). All of the vertical profiles were generally similar, with DI decreasing (lability decreasing) from surface waters to bottom waters. The highest observed DI was 4.89 (in the surface layer of station B7), and the lowest was 1.06 (in the bottom layer of station C3). Chl a was quite variable station-to-station (Fig. 5b). In the upper water column, nearshore stations B3 and C3 had much higher concentrations than did mid-shelf stations B7 and C6. Together, these stations indicated high primary production in the upper layers of nearshore waters. The lowest Chl a encountered was 0.56 mg m−3, at 2 m depth at station C6, where concentrations increased with depth. Chl a at station B7 was nearly constant, decreasing from 1.21 mg m−3 at 2 m depth to 0.99 mg m−3 at 30 m depth. No δ13C data were available for stations B3, C3, and C6. At station B7 (Fig. 5c), values ranged from −22.1‰ to −20.5‰, with little vertical variation. The average value (−21.3‰ ± 0.6‰) is close to the marinesource endmember. Together, the δ13C and DI profiles indicate that fresh marine biogenic particles at these nearshore and mid-shelf stations experienced selective degradation during settling and were not much affected by mixing with terrestrial matter. In suspended particles collected at stations B3, B7, C3, and C6, γ-Aba was below the detection limit; at stations B3 and B7, β-Ala was below the detection limit. 3.5. Bottom water: Dissolved oxygen During the 2006 cruise, a localized area of hypoxia (DO b 2 mg L−1, or b66.7 μmol L−1) was encountered at stations M2–3, M2–4, and M3–3, just off the Changjiang river mouth. The lowest concentration measured was 63.2 μmol L−1, at station M3–3. Higher concentrations of dissolved oxygen occurred in more nearshore areas, including Hangzhou Bay. 4. Discussion 4.1. Indicators of OM degradation state in surface sediments Low DI values (b0.50) indicate the presence of low lability, relatively degraded organic matter, perhaps due to riverine (terrestrial) input of more degraded or refractory organic material (Hedges et al., 1997; Burdige, 2007) or long-term oxic alteration (Hedges et al., 1999). High

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DI values (N0.50) indicate the presence of more labile organic matter, perhaps due to episodic input of fresh organic matter from marine primary production at the nearshore and mid-shelf stations (Zhou et al., 2008; Jiang et al., 2014) and better preservation of organic matter in the fine-grained sediments of the mud area south of Cheju Island (Deng et al., 2006; Xiang et al., 2006). In addition to DI, we also assessed two independent indicators of organic matter degradation in surface sediments and suspended particulate matter. One such indicator is the ratio of the non-protein amino acids γ-aminobutyric acid and β-alanine to their precursors, Glu and Asp, respectively (Fig. 4b–c). The ratio Asp/β-Ala was significantly positively correlated with DI (r = 0.372, p b 0.01, n = 47) in surface sediments and suspended particulate matter combined (Fig. 6a). However, the correlation between Glu/γ-Aba ratio and DI (surface sediments only) was not significant (Fig. 6b). Similarly, the correlation between Asp/β-Ala and DI was not significant for the case of surface sediments only. One reason for the lack of correlation might be related to source-material inputs (Dauwe and Middelburg, 1998). Across the Changjiang Estuary, sediments dominated by inputs from siliceous diatoms and those dominated by inputs from calcareous organisms mix to varying extents (Yu et al., 2013). The presence of carbonate-rich sediments may change the AA spectrum because of the enhanced adsorption capacities of carbonate surfaces for acidic amino acids (Carter and Mitterer, 1978; Ittekkot et al., 1984) — e.g., Asp and Glu. As a result, calcareous sediments may exhibit elevated Asp and Glu percentages. In addition, there is also the fact that Asp and Glu do not always produce β-Ala and γ-Aba during degradation (Cowie and Hedges, 1994). Therefore, depending on the composition of the biogenic sediments, Asp/β-Ala and Glu/γ-Aba ratios may not always be consistent with DI values in indicating degradation state. Another potential indicator of degradation state is the THAA/HA ratio (Dauwe and Middelburg, 1998) because HAs, compared to THAA yields, are relatively resistant to microbial decomposition. As degradation proceeds, then, the THAA/HA ratio would be expected to decrease. Within the Changjiang Estuary, DI was positively correlated with THAA/ HA (mg mg−1) (r = 0.464, p b 0.01, n = 46) in surface sediments and suspended particulate matter combined (Fig. 6c). This finding supports the notion that carbonate-rich sediments may skew indices that rely exclusively on acidic amino acids. We consider DI to be a more reliable indicator of degradation than simple ratios of AAs. The parameter DI, which has been successfully applied in other areas (Dauwe and Middelburg, 1998; Pantoja and Lee, 2003; Zhu et al., 2014; Hébert and Tremblay, 2017), robustly bundles or integrates information from a suite of amino acids (Eq. (3)). Single

Fig. 5. Vertical profiles of suspended particulates at stations B3, B7, C3, and C6: (a) degradation index, (b) chlorophyll a concentration, and (c) δ13C of particulate organic carbon. On panel (c), typical endmember values are also shown for terrestrial samples (Ft = 1) and marine samples (Ft = 0). Station locations are shown in Fig. 1.

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10

5

a

0 -9

30 5

THAA/HA (mg mg-1)

r = 0.372

15

35

6

sediments particles outliers

Glu/γ-Aba (mol% mol%-1)

Asp/β-Ala (mol% mol%-1)

20

4 3 2

-3

0

3

6

20 15 10 5

b

1 -6

r = 0.464

25

-9

c

0 -6

-3

0

3

6

-9

-6

-3

0

3

6

Fig. 6. Relationship between degradation index DI and (a) Glu/γ-Aba, (b) Asp/β-Ala, and (c) THAA/HA.

amino acids considered in isolation or in simple ratios may be more susceptible to environmental skewing (e.g., in the course of degradation and preservation) or analytical errors. 4.2. Sediment source (terrestrial versus marine) and OM degradation state Previously reported δ13C values for East China Sea surface sediments indicate that the Changjiang River supplies a large fraction of the marginal sea's organic matter, with some being transported as far away as the southern Okinawa Trough (Kao et al., 2003; Xing et al., 2011). Analyses of n-alkanes and polycyclic aromatic hydrocarbons have also indicated that terrestrial input dominates over marine inputs in the inner estuary's suspended and surface sediments (Sicre et al., 1993; Jeng and Huh, 2008). The two primary end-members of organic matter in East China Sea surface sediments can therefore be considered to be terrestrial matter, mainly from Changjiang River transport, and East China Sea marine autochthonous matter. We used a classical two-endmember model of OM δ13C signatures to estimate the fraction of terrestrial organic carbon, Ft, in the estuary sediments (Eq. (2)). Stations with Ft N 0.5 (dominated by terrestrial organic matter) were mostly located near the coast, while stations with Ft b 0.5 (dominated by marine organic matter) were located in the central part of the research area, along a southeast-northwest–trending belt (Fig. 4d). Seaward of this belt, some deep offshore stations — e.g., stations C14–9 (Ft = 0.50) and C18–6 (Ft = 0.54) — had even more terrestrial material than some of the shallower stations, indicating that terrestrial POC had been transported offshore across the shelf from the coast (Milliman et al., 1989; Zeng et al., 2015). Plotting DI as a function of Ft and dividing the graph into quadrants (using DI = 0.50 and Ft = 0.5 as the defining boundaries) allows the Changjiang Estuary sediments to be classified into four types (Fig. 7a): (1) TL, terrestrial labile; (2) ML, marine labile; (3) MR, marine refractory; and (4) TR, terrestrial refractory. Overall, most sediments fell into the TR, ML, and MR quadrants. Consistent with studies in other coastal areas (Cowie and Hedges, 1992; Aller et al., 1996; Aller and Blair, 2004; Burdige, 2007), fresh/labile terrestrial material (TL) was rare. In the Ft data set, 7 outlier stations were identified using the boxplot procedure (Sim et al., 2005) of the SPSS® 13 software: stations M1–1, M4–1, M4–5, M5–1, M5–7, O5–8 and O7–14. After removal of these outliers, linear regression (Fig. 7b) yields: DI ¼ ð−4:723 1:357Þ F t þ ð0:372 0:526Þ

ð4Þ

The two variables DI and Ft are significantly inversely correlated (r = −0.50, R2 = 0.25, p b 0.01, n = 38). The parameter Ft explains 25% of the total observed DI variability. The fact that DI increases with decreasing Ft indicates that relatively fresh/labile organic matter (high DI) was generally of marine origin. When Ft = 0, the sedimentary organic matter would have a DI of 0.372 ± 0.526. This marine DI is similar to the value encountered in sandy sediments at the North Sea station BF of Dauwe and Middelburg (1998) (DI = 0.25), where their observations of highest primary production occurred. These DI values are also similar to the values Dauwe and Middelburg (1998) determined for the labile source materials: phytoplankton, bacteria, and sediment trap material. When Ft = 1 (no marine contribution), DI would be −4.35 ± 1.46. This value is similar to the DI of the oxidized turbidite of (Dauwe and Middelburg, 1998) (DI = −3.47). Some stations with mainly marine-source (low Ft) sediments (e.g., stations O7–14, O7–6, and O5–8, just outside the Zhoushan Islands) had lower DI scores than other marine stations. Similarly, sediments in the shelf area between 50 and 100 m depth (i.e., in the flow path of the Taiwan Warm Current) had a deep-ocean character in that they contained relatively little OC (Supplemental Table 1). This OC was highly degraded, likely due to long-term reaction with O2, as described by (Hedges and Keil, 1995). 4.3. OM degradation under different oxygen conditions Assuming that seasonal patterns of oxygen distribution and hypoxia duration have been similar in recent years (Wei et al., 2007; Zhu et al., 2011; Zhu et al., 2016), the surface sediments we sampled would be exposed to fluctuations in bottom water oxygen concentrations. Because apparent oxygen utilization (AOU = [O2]saturation − [O2]measured) contains more information about long-term aerobic degradation than does instantaneous DO concentration, we used AOU to represent oxygen utilization by microorganisms during their degradation of organic matter in the water column and in sediment pore waters. Multiple linear regression on the Changjiang Estuary data yields: DI ¼ ð−2:515 1:259Þ F t þ ð0:0109 0:005Þ AOUbot −ð1:362 0:802Þ

ð5Þ

where AOUbot is bottom-water AOU. The negative correlation between DI and Ft indicates that fresh/labile organic matter was generally of marine origin, while the positive correlation between DI and AOUbot, indicates that the respiration of more labile organic matter acted to significantly elevated oxygen consumption. Comparison of the


DI

4

ML

4

TL

2

2

0

0

-2

-2

-4

-4

-6 -8 0.0

MR

-6

TR

a

Regression Outlier

.2

.4

.6

.8

1.0

Ft

-8 0.0

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r = -0.50 DI = -4.723* Ft + 0.372

Regression line 95% confidence Prediction line

.2

b

.4

.6

.8

1.0

Ft

Fig. 7. Relationship between degradation index DI and fraction of terrestrial organic matter Ft: (a) categorization of all Changjiang Estuary sediment samples and (b) linear regression, excluding the 7 outlier data points.

standardized coefficients (−0.34 and 0.37) indicates that the influence of AOUbot on DI was greater than that of Ft. The correlations between Ft and AOUbot and DI were significant (R2 = 0.389, p b 0.01, n = 32), with 39% of the DI variability being explained by Ft and AOUbot together. To further explore differences in AA composition and other sediment characteristics in relation to water-column oxygen, we categorized the Changjiang stations according to AOU conditions. Because AOU was significantly correlated with DO (i.e., AOU = −1.0027 * DO +224.75; r = −0.97, p b 0.01, n = 144), We characterized each station in terms of these 3 categories: hypoxic (AOU N 130 μmol L−1, equivalent to DO b3 mg L−1), semi-oxic (130 N AOU N 68 μmol L−1, equivalent to 3 b DO b5 mg L−1), and oxic (AOU b 68 μmol L−1, equivalent to DO N5 mg L−1). Mean DI was highest in the hypoxic category (−0.21 ± 1.08) and lowest in the oxic category (−2.09 ± 1.57). In other words, organic matter was most labile in hypoxic areas and least labile in welloxygenated areas. The difference between the two average DI values was significant (t-test, p b 0.01). In contrast, values of OC and TN in the hypoxic category were not significantly different from values in the other two categories (Supplemental Table 2, t-test, p N 0.05); the same was true for THAA and HA. Overall, AOU was not significantly correlated with OC, TN, THAA, or HA. The highest levels of these constituents occurred at stations with abundant faunal biomass (unpublished data). The apparent preservation of this organic matter in the presence of oxygen-dependent animal life and low AOU indicates that oxygen is not the only important factor controlling OM degradation and preservation (similar to the observations of Vandewiele et al., (2009) in the Pakistan margin oxygen minimum zone). From the significant inverse correlation between AOUbot and Ft (r = −0.49, R2 = 0.24, p b 0.01, n = 144), it can be inferred that organic matter in the hypoxic areas was mostly derived from marine sources. Where AOU N 130, average Ft = 0.408 ± 0.161. The decomposition of autochthonous marine particles in the water column and on the sea floor may result in low bottom-water oxygen even at coastal stations with a relatively high fraction of terrestrial organic matter (e.g., stations M1–1, M2–1, and M2–2, near the Changjiang river mouth). Terrestrial organic matter may also be decomposed, thus consuming oxygen, but this process was likely very limited because of this material's high degradation status (e.g., in the coastal high-oxygen

area) and refractory nature (Hedges et al., 1997). Occurrences of coastal hypoxia may be partly due to the reworking of buried sediments under strong tidal influence or bioturbation and irrigation, with significant oxygen being consumed during “oxic-anoxic-oxic” redox transitions (Hulthe et al., 1998). Spatial differences in molar percentages of the aromatic amino acid Tyr, which is inherently labile (Jennerjahn and Ittekkot, 1997; Dauwe and Middelburg, 1998), could also be an indication of differences in redox-related OM alteration, which would in turn be influenced by the duration of exposure to molecular oxygen (Suthhof et al., 2000). In our samples, however, Tyr was not significantly correlated with bottom DO or AOUbot. Tyr was significantly correlated with DI (r = 0.407, p b 0.01, n = 31, after excluding samples where Tyr = 0), with fresher OM (higher DI) containing more Tyr than degraded OM. The highest proportions of this amino acid occurred in sediments in the hypoxic category, this association of Tyr with hypoxia is consistent with reports from other areas (Nissenbaum et al., 1972; Haugen and Lichtentaler, 1991; Suthhof et al., 2000). The lowest Tyr values occurred in oxic areas, this pattern again suggests the presence of relatively fresh OM in the hypoxic areas. The presence of abundant bacteria may also contribute to an increase in the Tyr percentage (Suthhof et al., 2000; Hébert and Tremblay, 2017), but data regarding bacterial amino acids are lacking. High rates of productivity and biogenic particle accumulation in hypoxic areas may additionally contribute to relatively high sedimentary Tyr values because of the abundant OM thus supplied to the benthic bacterial community. 4.4. OM degradation and grain size Sediment grain size distributions were different in the different AOU areas (Supplemental Table 2), and such differences may also play a role in determining organic matter degradation state. Most of hypoxic category sediment samples were collected from the Changjiang estuary mud area (Guo et al., 2003) located east of Shanghai. This area is characterized by a dominance of silt and clay (e.g., core CJ43 of (Zhao et al., 2015)) and a high sedimentation rate (e.g., station DEB5 of (Liu et al., 2006), with a sedimentation rate of 2.14 cm yr−1). Sediments of the semi-oxic category came mostly from the sandy-sediments area of Qin et al. (1987) or the residual sedimentary area of (Wang, 1995). Sediments of the oxic category came mostly from the coastal area of modern

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sedimentation (Wang, 1995) and some parts of the middle and outer shelf. These patterns suggest that organic matter may be best preserved in silt-and-clay–dominated hypoxic areas, as evidenced by the relatively high average DI in these areas. Supporting evidence is offered by the significantly negative correlation of OC (r = −0.580, p b 0.01, n = 36), TN (r = −0.471, p b 0.01, n = 30), THAA (r = −0.623, p b 0.01, n = 38), and HA (r = −0.641, p b 0.01, n = 38) with sand percentages. The key factor is probably the greater mineral surface area available for organic matter sorption onto silt and clay sediments as compared to sandy sediments (Hedges and Keil, 1995). This mechanism would be consistent with the findings of previous work conducted in the Changjiang Estuary (Hu et al., 2012).

other areas. In future work, additional biogeochemical indicators (e.g., sugars, lignin, fatty acids) should be used to more specifically identify organic matter sources in efforts to explain variations of OM degradation. Oxygen exposure times of the sediments should also be determined to explore the effects of oxic environment on the alteration of organic matter reactivity. With additional information about OM quality and nutritional character, insights in to implications for benthic animals could also be gleaned. Such refinements could help build a better understanding of the mechanisms of organic matter utilization, degradation, preservation and burial in not only the Changjiang Estuary but also other estuarine ecosystems. This improved understanding is especially important in the global context of increasingly frequent and extensive episodes of estuarine hypoxia and acidification.

4.5. Implications for benthic fauna Amino acids are components of proteins, vital for the production of enzymes and structural materials within marine organisms such as deposit-feeding invertebrates and benthic macrofauna (Phillips, 1984). AAs also serve as sources of nitrogen and carbon for primary producers (McCarthy et al., 2013), whose products eventually support benthic consumers. Previous studies of the spatial distributions of benthic biomass (Wang et al., 2009; Wang et al., 2012) and macrobenthos abundance (Liu et al., 2008; Shou et al., 2013) within the Changjiang Estuary clearly show high biomass concentrated between 122°E and 123°E, between the 20 and 50 m isobaths. This pattern is with the distributions of THAA (Fig. 3a) and DI in our surface sediments (Fig.4a). Together, these distributions suggest that benthic fauna prefer areas where AAs are abundant and more labile organic matter available as a valuable food source. Some essential amino acids (EAAs), including Thr, Val, Met, Ileu, Leu, Phe, His, Lys, and Arg, cannot be made by animals and must be obtained from external foods (Phillips, 1984). Deficiencies of available EAAs will therefore limit the growth of benthic animals. Due to the lack of THAA data for Changjiang Estuary benthic organisms, we cannot evaluate whether any EAAs would limit the need of the local benthos.

Acknowledgements The authors would like to thank the crew of the research vessel Haijian 49 for their support in sampling and logistics. We also thank D. Xu, L. M. Ye, X. G. Yu (Second Institute of Oceanography, State Oceanic Administration), and W. J. Cai (University of Delaware) for their technical support and helpful comments. This study was jointly supported by the National Natural Science Foundation of China (No. U1709201, U1609201, 91128212, 41203085, 41206085, 41106050, 40403013); the Scientific Research Fund of the Second Institute of Oceanography, State Oceanic Administration, China (No. JT1603); the Natural Science Project of Zhejiang Province (No. Y5110171). The field data analyzed in this study may be obtained by contacting the corresponding author ([email protected]). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2018.04.242.

References 5. Conclusions For the first time, 17 individual amino acids were analyzed and then collectively characterized to describe organic matter degradation state in surface sediments and suspended particulates of the Changjiang Estuary, as quantitatively expressed by the degradation index DI. As expected, surface sediments were generally more degraded than suspended particles. OM degradation state in surface sediments was 39% associated with source material and bottom water apparent oxygen utilization together, with the influence of AOUbot being greater than that of Ft. Relatively fresh/labile organic matter was generally associated with marine sources, whereas relatively old/refractory matter was generally associated with terrestrial sources. More labile material served to elevate oxygen consumption in bottom waters. DI and the labile amino acid Tyr were highest in hypoxic areas, probably due to a combination of fresh marine inputs plus OM preservation in fine-grained sediments. We consider DI, which relies on a broad suite of AAs, to be the most reliable indicator of degradation state of organic matter in a wide range of marine environments. In the Changjiang Estuary, the indicators Asp/ β-Ala ratio and THAA/HA ratio may provide more convenient and affordable means of accessing organic matter degradation status when analytical constraints preclude the use of the full-suite DI. However, variations of other potential indicators of degradation state (e.g., Glu/γAba, HA molar percentages) did not consistently match the variations of DI. The approaches we used to explore the relationships between terrestrial, marine, sedimentary, and water-column components and processes (i.e., DI principal component analysis, multiple linear regression, and an isotope mixing model) could be fruitfully applied to

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