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The sources and composition of organic matter in sediments of the Jiaozhou Bay: implications for environmental changes on a centennial time scale
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Xuming KANG1, 2, Jinming SONG1, 2, 3, *, Huamao YUAN1, 2, 3, Xuegang LI1, 2, 3, Ning LI1, 2, 3, Liqin DUAN1, 2, 3
Acta Oceanologica Sinica | 2017, 36(11) : 68 - 78
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Acta Oceanologica Sinica | 2017, 36(11): 68-78
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The sources and composition of organic matter in sediments of the Jiaozhou Bay: implications for environmental changes on a centennial time scale
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Xuming KANG1, 2, Jinming SONG1, 2, 3, *, Huamao YUAN1, 2, 3, Xuegang LI1, 2, 3, Ning LI1, 2, 3, Liqin DUAN1, 2, 3
Affiliations
  • 1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  • 2 Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
  • 3 University of Chinese Academy of Sciences, Beijing 100049, China
Published: 2017-11-01 doi: 10.1007/s13131-017-1076-1
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The Jiaozhou Bay is characterized by heavy eutrophication that is associated with intensive anthropogenic activities. Four core sediments from the Jiaozhou Bay are analyzed using bulk technologies, including sedimentary total organic carbon (TOC), total nitrogen (TN), the stable carbon (δ13C) and nitrogen (δ15N) isotopic composition to obtain the comprehensive understanding of the source and composition of sedimentary organic matter and further shed light on the environmental changes of the Jiaozhou Bay on a centennial time scale. Results suggest that the TOC and TN concentrations increase in the upper core, having indicated a probable eutrophication process since the 1920s in the inner bay and the 2000s in the bay mouth. The TOC and TN concentrations outside the bay have also changed since 1916 owing to the variation of terrigenous input. Considering TOC/TN ratio, δ13C and δ15N, it can be concluded there is a mixture of terrigenous and marine organic matter sources in the study area. A simple two end-member (terrigenous and marine) mixing model using δ13C indicats that 45%–79% of TOC in the Jiaozhou Bay is from the marine source. The environmental changes of the Jiaozhou Bay are recorded by geochemical proxies, which are influenced by the intensive anthropogenic activities (e.g., extensive use of fertilizers, and discharge of sewage) and climate changes (e.g., rainfall).

organic matter  /  sources  /  anthropogenic activities  /  environmental changes  /  sediments  /  Jiaozhou Bay
Xuming KANG, Jinming SONG, Huamao YUAN, Xuegang LI, Ning LI, Liqin DUAN. The sources and composition of organic matter in sediments of the Jiaozhou Bay: implications for environmental changes on a centennial time scale[J]. Acta Oceanologica Sinica, 2017 , 36 (11) : 68 -78 . DOI: 10.1007/s13131-017-1076-1
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1 Introduction
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The burial of organic matter in coastal and shelf sediments plays a key role in regulating the global carbon cycle, and up to 80% of organic matter is buried in shallow marine ecosystems (Berner, 1982). The coastal margins, especially those under significant river influence, are characterized by complex biogeochemical patterns of sedimentary organic matter due to significant land-sea exchange of materials along with anthropogenic impact (Gao et al., 2012; Wang et al., 2013). Knowledge of the sources and composition of organic matter in estuarine and coastal sediments and factors in controlling its distribution is important for the understanding of global biogeochemical cycles (Wang et al., 2013; Li et al., 2015a, b). Moreover, the exploration of the geochemical behavior of sedimentary organic matter is important for a better understanding of its responses to regional climate changes and anthropogenic impact (Bianchi and Allison, 2009; Wang et al., 2013; Hu et al., 2016).
As bulk parameters, TOC/TN ratios and the isotope compositions of carbon (δ13C) and nitrogen (δ15N) are reliable proxies in the study of the sources and composition of organic matter buried in marine sediments, which could help us to understand the environmental changes in coastal systems (Cohen and Fong, 2005; Henderson and Holmes, 2009; Wang et al., 2013; Hu et al., 2016; Ke et al., 2017). The use of these parameters relies on the differences among the natural abundance of δ13C, δ15N and TOC/TN ratio in organic matter from different sources (Gao et al., 2012). In general, organic matter of the marine source and the terrigenous source had a TOC/TN ratio of approximately 4–10 and greater than 20, respectively (Meyers, 1994; Li et al., 2008). However, post-depositional changes in this ratio could occur (Meyers, 1994), which would result in the inaccuracy of source identification. In contrast to TOC/TN ratios, δ13C only changed slightly during the sedimentation and degradation (Wang et al., 2013). Terrigenous organic matter generally exhibited more depleted δ13C (<–27‰) relative to marine organic matter (–22‰) (Meyers, 1994). The δ13C usually increased with increasing productivity (Hodell and Schelske, 1998). The δ15N was commonly used to track anthropogenic nitrogen pollution, and varied significantly in different contaminants (Wang et al., 2013), ranging from –2‰ to 4‰ in nitrogen fertilizers and from 10‰ to 20‰ in human and animal manure (Ke et al., 2017). Moreover, δ15N in sediments could be used to reflect the deposition rates of organic matter and origins of nitrogen in phytoplankton and mineralization process (Cohen and Fong, 2005; Wang et al., 2013). Therefore, the combination of these three parameters could help us better discriminate organic matter sources in coastal areas (Meyers, 1994).
Owing to the interference of the anthropogenic activities (e.g., rapid human population growth, rapid urbanization, excessive use of agricultural fertilizers, increasing sewage discharge, intensive mariculture and land reclamation) and climate changes, severe environmental problems including eutrophication, organic matter accumulation and heavy metal pollution occurred in China’s coastal waters and lakes (Shen et al., 2005; Dai et al., 2007a; Liu et al., 2010b; Wang et al., 2013; Li et al., 2014, 2015a, b ; Lin et al., 2015; Yuan et al., 2016). Consequently, the nature balance between the production and decomposition of organic matter has been disturbed in many coastal areas (Yang et al., 2011; Gao et al., 2012; Wang et al., 2013). Understanding the sources of anthropogenic inputs and the coupled impacts from the anthropogenic activities and the climate changes on ecosystems is therefore a major environmental concern.
Over the last 150 a, with the rapid economic and social development in Qingdao City, the Jiaozhou Bay has been largely affected by the anthropogenic activities, and increasing amounts of industrial, agricultural and aquaculture waste have been discharged into the Jiaozhou Bay (Li et al., 2008). Moreover, climate changes, including the temperature increase and the rainfall decrease were reported (Yuan et al., 2016). As a result of the anthropogenic activities and the climate changes, eutrophication and harmful algal blooms occurred frequently (Liu et al., 2010b; Yuan et al., 2016). These changes, in turn, have the potential to alter the nature and content of organic matter of marine deposits and their TOC/TN ratio, δ13C and δ15N values (Gao et al., 2012). There are plenty of reports on eco-environment feedback of the Jiaozhou Bay to anthropogenic activities (Dai et al., 2007a; Liu et al., 2010b), such as the nutrient structure and phytoplankton community compositions (Shen, 2001), the heavy metal pollution (Li et al., 2011), the burial of biogenic element (Dai et al., 2007b; Wang et al., 2017) and the sedimentary dynamics (Zhao et al., 2015), etc. However, the study on organic matter sources and distribution in this region is scarce and the past study was simply based on the TOC/TN ratio or single core sediment (Li et al., 2008; Yang et al., 2011). Moreover, the impact of anthropogenic disturbance on environmental changes on a centennial time scale is still unclear in the Jiaozhou Bay. Therefore, in this study, the TOC/TN ratio, δ13C and δ15N values were combined to present a comprehensive picture of the sources and composition of organic matter buried in the Jiaozhou Bay sediments. In addition, the present study intended to further address the hypothesis that the environment is significantly influenced by intensive anthropogenic activities and climate changes.
2 Materials and methods
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2.1 Study area
The Jiaozhou Bay is a semi-enclosed bay, located on the western coast of the Yellow Sea, which is adjacent to Qingdao City (Fig. 1). The bay has a total area of approximate 390 km2, with a mean depth of 6–7 m (Dai et al., 2007a, b). The Jiaozhou Bay lies in a warm temperature monsoon climate zone, with an average annual air temperature of 12.3°C and rainfall of 725–1 100 mm (Yuan et al., 2016). There are more than ten small rivers (e.g., Yanghe River, Dagu River, and Licun River) discharging into the Jiaozhou Bay with industrial and domestic sewage and sediments. Moreover, there are large coastal areas of mariculture ponds along the bay for fish, shrimp and shellfish culture. The annual discharge of terrigenous dissolved inorganic nitrogen increased by ten times from the 1980s to the 2000s (Wang, 2009; Yuan et al., 2016), which induced the algae blooms, the depletion of fish biodiversity and ecosystem degradation in the Jiaozhou Bay in recent years (Li et al., 2008; Lu et al., 2017; Yuan et al., 2016).
2.2 Sampling
Field expeditions, aboard the R/V Kexue 3, were carried out in the Jiaozhou Bay during June 2015. Four gravity cores were retrieved from the inner, mouth and outside of the bay, respectively (Fig. 1). Cores C3 and C4 were collected in the inner bay, with the water depths of 13 and 10 m, respectively, and consisted of clay silt. Cores C5 and C6 were sampled in the mouth and outside of the bay, with the water depths of 21 and 22 m, respectively. The sediment type of them was sandy silt. The core was sliced into 2 cm-thick segments and immediately placed in plastic zip lock bags with air being excluded. All samples were stored in the dark at –20°C in the laboratory for further analysis.
2.3 Bulk parameters (TOC, TN, δ13C, δ15N and porosity)
Samples for TOC, TN, and stable carbon (δ13C) and nitrogen (δ15N) isotopes of organic matter were measured at Third Institute of Oceanography, State Oceanic Administration, China. TOC and TN of sediment samples were analyzed using a Vario El-Ш elemental analyzer, following the method of Hu et al. (2014). Briefly, sediment samples were ground in an agate mortar after being dried, and then soaked in 1 mol/dm3 HCl at the room temperature for 1 d to remove carbonates. After rinsing with Milli-Q water several times and drying in an oven at 60°C, the carbonate-free samples were measured for the TOC and TN concentrations. Replicate analysis of well-mixed samples provided a standard deviation of 0.01% for the TOC and TN concentrations (n=5). The δ13C and δ15N analysis was performed on inorganic carbon-free sediments, using a Thermo Deltaplus XL continuous flow mass spectrometer. The values of δ13C and δ15N were expressed in a standard delta notation relative to Pee Dee Belemnite (PDB) and air, respectively. The average standard deviations of δ13C and δ15N based on the replicated analysis were 0.1‰ (n=5). Porosity was determined by a mass difference before and after the drying of the sediments.
2.4 Sediment ages and burial flux of organic carbon
Sediments of Core C4 were dated using 210Pb radionuclide. 210Pb was measured via its grandparent 210Po. The method was described in detail in Huh et al. (1997). In brief, 0.5 g of sediments for each aliquot was digested with concentrated HNO3 after adding an accurate 209Po spike as yield monitor. Both 210Po and 209Po in solution were finally auto-deposited on a silver-plate under specific conditions. The activities of Polonium isotopes（i.e., 210Po and 209Po）were counted using α- spectrometry (ORTEC). The sedimentation rate of Core C4 was calculated by excess 210Pb with a widely used constant initial concentration (CIC) model (Dai et al., 2007a). Considering locations of sediment Cores C3 (36.113°N, 120.235°E), C5 (36.020°N, 120.272°E) and C6 (35.978°N, 120.452°E) were close to the sampling stations of J37 (36.123°N, 120.222°E), D4 (36.019°N, 120.259°E) and J94 (35.977°N, 120.452°E) collected in the Jiaozhou Bay during 2003 in the published studies of our group (Qi, 2005; Dai et al., 2007a; Li et al., 2011). The sedimentation rate had been constant during these several years owing to the stable sedimentary environment in the Jiaozhou Bay (Liu et al., 2010a). Therefore, the sedimentation rates of J37, D4 and J94 in previous studies were employed in this study. The burial flux of organic carbon was calculated according to Li et al. (2008).
2.5 Statistical analyses
All statistical tests were performed using SPSS 16.0 software. Before each statistical analysis, Shapiro and Bartlett tests were performed to test the data set normality and homoscedasticity, respectively. One-way ANOVA was applied on data sets following normal distributions and showing homogeneous variances. The one-way ANOVA was used to determine the differences of the parameters between two stations. For all statistical tests, a probability (P) of 0.05 was used to show the statistical significance.
3 Results and discussion
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3.1 Sedimentation rate
The 210Pb and excess 210Pb activities were plotted on a log scale against depth (Fig. 2). The excess 210Pb values show a negative trend with an increasing depth for Cores C3 (r=–0.82, P<0.05), C4 (r=–0.82, P<0.001) and C6 (r=–0.99, P<0.01). While the excess 210Pb values exhibit a fluctuating trend with the increasing depth for Core C5. According to the CIC model, the average sedimentation rate of Core C4 was calculated to 0.28 cm/a. The sedimentation rate from previous investigations was 0.64 cm/a for Core C3, 1.63 cm/a in the above 38 cm and 3.96 cm/a below 38 cm for Core C5, and 0.45 cm/a for Core C6, respectively. According to the sedimentation rates, the chronologies for Cores C3, C4, C5 and C6 were ca. 1923–2015, 1726–2015, 1980–2015 and 1777–2015, respectively.
The sedimentation rates (0.28 cm/a) of Core C4 were relatively lower than those (0.64 cm/a) of Core C3 due to their different geographic positions. Core C4 occupies the cross of two main channels, namely Cangkou Channel and Hongdao Channel, where a current velocity is high during a tidal fluctuation. Fine sediments were difficult to deposit under the high current velocity (Qi, 2005). Compared with Cores C3, C4 and C6, Core C5 shows much higher sedimentation rates (1.63 cm/a above 38 cm and 3.96 cm/a below 38 cm). The higher sedimentation rates in Core C5 were related to large amounts of terrigenous material input and serious coastal erosion (Qi, 2005; Wang et al., 2006). The sedimentary environment changed in this area with the variation of terrigenous material input. The sedimentation rate decreased by 59% in recent decades owing to the decline of terrigenous material input (Qi, 2005).
3.2 Geochemical parameters in sediments of the Jiaozhou Bay
TOC and TN contents range from 0.14% to 0.41% and 0.02% to 0.05% in core C3, respectively. Both TOC and TN contents have displayed an increasing trend with time since 1923, with r=0.92 (P<0.01) for TOC and r=0.91 (P<0.01) for TN, respectively, especially in recent 15 a (upper 10 cm) (Figs 3a1 and a3), implying a heavy eutrophication in this site. The burial flux of TOC has ranged from 3.63 to 6.77 mmol/(m2·d), and displayed an increasing trend with time since 1923 (r=0.91, P<0.01) (Fig. 3a2). The TOC/TN ratios varied from 8.2 to 11.5, displaying an increasing trend with time since 1923 (r=0.72, P<0.01) (Fig. 3a4). δ13C and δ15N ranged from –22.2‰ to –20.4‰ and from 9.7‰ to 15.7‰, respectively. Both of them have presented a decreasing trend with time since 1923 (r=0.70, P<0.01) (Figs 3a5 and a6).
Core C4 is also located in the inner bay and close to the eastern coast of the Jiaozhou Bay. TOC and TN contents in core C4 ranged from 0.34% to 0.74% and 0.03% to 0.05%, respectively, which are significantly higher than those in Core C3 (One-way ANOVA, P<0.05). Generally, a grain size is a major factor in controlling the spatial variations of TOC and TN (Gao et al., 2012). In this study, the porosity data were used to compare the differences of the grain size between these two cores, considering the fine-grained sediments tending to have higher porosities than coarser sediments (Buckingham, 2005). The results indicate that there is no significant difference in the porosity between Cores C3 and C4 (One-way ANOVA, P>0.05), implying that the grain size is not the main factor in determining organic matter contents in the Jiaozhou Bay. Besides, TOC/TN ratio of Core C3 (8.2–11.5) was significantly lower than that (11.4–16.4) in core C4 (One-way ANOVA, P<0.05). Babbin et al. (2014) suggested that organic matter could easily decompose under the relatively low TOC/TN ratio. The TOC contents in Core C4 vary with time before 1919 (r=–0.32, P>0.05) and then have presented an increasing trend since 1919 (r=0.76, P<0.05) (Fig. 3b1). The increasing TOC from 1748 to 1812 might be related to the increasing terrigenous input, which was proved by the decreased δ13C. The burial flux of TOC range from 2.39 to 5.75 mmol/(m2·d), and displayed an increasing trend with time since 1919 (r=0.79, P<0.05) (Fig. 3b2). TN presents a decreasing trend with time before 1919 (r=–0.74, P<0.01), but an increasing trend since that time (r=0.79, P<0.05) (Fig. 3b3). The TOC/TN ratio varies with time before 1919, but a decreasing trend has occurred since 1919 (r=–0.88, P<0.01) (Fig. 3b4). The δ13C and δ15N range from –22.8‰ to –21.8‰ and from 7.2‰ to 17.6‰, respectively. The δ13C presents two decreasing trends with time before 1919 (r=–0.72, P<0.05) and since 1983 (r=–0.93, P<0.05). An increasing trend of δ13C occurred from 1919 to 1962 (r=0.99, P<0.05), suggesting the variation of terrigenous organic matter (Fig. 3b5). Moreover, the decreased δ13C might be related to the wide growth of Core C3 plant with δ13C of –26‰ to –27‰ (Wang et al., 2013) in northern China during this period. There were two increasing trends of δ15N with time before 1919 (r=0.79, P<0.01) and since 1983 (r=0.91, P<0.05) (Fig. 3b6).
Station C5 is located in the mouth of the Jiaozhou Bay, which is more adjacent to Huangdao and Qingdao Cities than other three stations (Fig. 1). The TOC and TN contents are 0.30% to 0.82% and 0.03% to 0.07%, respectively. The relatively high TOC and TN contents might be related to the high sedimentation rate at this station, which is beneficial to the preservation of organic matter (Ingall and van Cappellen, 1990). Both TOC and TN contents vary with time before 2003, but an increasing trend occurred since 2003 (r=0.74, P<0.05 for TOC and r=0.80, P<0.05 for TN) (Figs 3c1 and c3). The burial flux of TOC ranges from 14.74 to 82.12 mmol/(m2·d), and displays a sharp decrease after 1992 (Fig. 3c2). The TOC/TN ratio ranges from 10.3 to 14.4, and has presented a decreasing trend with time since the 1980s (r=–0.50, P<0.05) (Fig. 3c4). The δ13C and δ15N values range from –22.2‰ to –18.6‰ and from 6.6‰ to 13.0‰, respectively. The δ13C presents a decreasing trend with time since the 1980s (r=–0.72, P<0.01), whereas the δ15N presents an increasing trend with time after the 1980s (r=0.56, P<0.05) (Figs 3c5 and c6). The decreased δ13C and increased δ15N imply the intensive terrigenous input in this site. The high TN contents and a significant correlation between δ13C and δ15N (r=–0.66, P<0.05; Table 1) also indicated the high nitrogen loadings at this station.
Compared with Cores C3, C4 and C5, the lower and less variable TOC (0.18%–0.30%) and TN (0.02%–0.03%) contents were observed in core C6, which probably resulted from the little riverine input. Sediments in this area came from the Jiaozhou Bay, which were carried by the tidal and coastal current (Qi, 2005). The TOC and TN contents varied with the time before and since 1916 (Figs 3d1 and d3). The decrease of TOC and TN contents since 1916 might be related to the dilution by increased terrigenous material. It could be proved by the changed δ13C signal (ranging from –22.6‰ to –21.3‰). Prior to 1916, δ13C varies with time, but a decreasing trend have occurred since 1916 (r=–0.72, P<0.05) (Fig. 3d5). The burial flux of TOC ranges from 2.76–4.64 mmol/(m2·d), and displays a similar trend as TOC (Fig. 3d2). The TOC/TN ratio ranges between 9.6 and 11.9, which varies with time before 1942 and has decreased since 1942 (r=–0.90, P<0.01) (Fig. 3d4). The δ15N ranges from 4.8‰ to 16.8‰, which varies with time before 1916 and has decreased since 1916 (r=–0.82, P<0.01) (Fig. 3d6). The δ15N shows higher values in Core C6 before 1950, implying a clear nitrogen input during that period. The high nitrogen input promoted the increase of productivity and consequently induced the high δ15N before 1950. Teranes and Bernasconi (2000) suggest that the increasing productivity is likely to induce the decrease of surface dissolved inorganic nitrogen and the increase of δ15N values. The decrease of δ13C and δ15N since 1916 has indicated that the outside bay is suffering from an increasing influence from the terrigenous input.
3.3 Sources and composition of organic matter in sediments of the Jiaozhou Bay
The TOC/TN ratio and δ13C have been widely used to distinguish marine sources and terrigenous sources of organic matter (Hu et al., 2013; Ke et al., 2017). The TOC/TN ratios of organic matter >20 and between 4 and 10 were from terrigenous and marine sources, respectively (Meyers, 1994; Li et al., 2008). The δ13C for terrigenous and marine sources is –26‰ and –19‰, respectively (Yang et al., 2011). Significant correlations existe between TOC and TN contents in four cores (Table 1), indicating that the influence of the sorption of inorganic nitrogen on organic matter was minimal (Hu et al., 2013; Li et al., 2015a, b). The significant correlations between the TOC/TN ratio and δ13C in three studied cores (P<0.01 for Core C3; P<0.05 for Cores C4 and C6) indicate that these two parameters can be used to identify the sources of organic matter in Cores C3, C4 and C6. Organic matter in the Jiaozhou Bay exhibits a range of TOC/TN ratio (8.2–16.4) and δ13C values (–18.6‰ to –22.8‰) indicative of mixed source inputs from marine and terrigenous materials. It was noteworthy that the single terrigenous input could also result in the corresponding δ13C (–18.6‰ to –22.8‰). For example, the mixture of terrigenous C3 (–26‰ to –27‰) and C4 (–9‰ to –16‰) plants could result in a δ13C value of –22‰ (Wang et al., 2013). However, although corn is the primary C4 plant in northern China, the influence of terrigenous C4 plant on organic matter could be neglected for its higher TOC/TN ratio (60–200) compared with organic matter (TOC/TN ratio being less than 17) in the Jiaozhou Bay. Therefore, it was reasonable that organic matter in the Jiaozhou Bay was a mixture of marine and terrigenous origins, which was consistent with previous studies of the Jiaozhou Bay (Li et al., 2008; Yang et al., 2011).
Various end-member mixing models have been successfully used to study the variation of different sources of organic matter inputs in aquatic systems (Yang et al., 2011; Li et al., 2015a, b). Here, we employed a two end-member mixing model using δ13C as source markers to distinguish the relative contribution of terrigenous and marine organic carbon in the Jiaozhou Bay, which assumed discrete δ13C values for terrigenous and marine end-member carbon (Liu et al., 2015). Another important assumption here is that end-member values have not changed significantly over the period of time examined in this study. The calculation of terrigenous and marine source (fT and fM) organic carbon contribution (Yang et al., 2011) was gained based on the following equations:
f T = δ 13 C M − δ 13 C S δ 13 C M − δ 13 C T ,,
f M =1− f T ,
On the basis of a previous study of the Jiaozhou Bay (Yang et al., 2011), the end-members values of δ13C for terrigenous and marine source (δ13CT and δ13CM) were –26‰ and –19‰, respectively. δ13CS was the values in the core samples.
The results of the two end-member model show that marine organic carbon is the dominant component of sedimentary TOC in four cores, and vary from 54% to 80%, 45% to 61%, 55% to 79% and 49% to 68% in Cores C3, C4, C5 and C6, respectively. Generally, the relative contributions from different sources were generally stable before the 1960s in the inner bay. After the 1960s, the contribution of terrigenous TOC has showed an increasing trend in Cores C3 and C4 since 1964 (r=0.67, P<0.05) and 1962 (r=0.88, P<0.05), respectively (Figs 4a and b). The relative contributions from marine TOC decreased (Figs 4a and b). The terrigenous TOC has presented an increasing trend in Cores C5 and C6 since 2003 (r=0.76, P<0.05) and 1955 (r=0.71, P<0.05), respectively (Figs 4c and d). The increasing TOC/TN ratio and decreasing δ13C in the same period also imply an increase in the input of terrigenous organic matter (Fig. 3). Moreover, depleted sedimentary δ13C corresponds to higher TOC contents, and a clear negative relationship is observed in Core C3 (r=–0.799, P<0.01). In a semienclosed system, the increased terrigenous input related to the intensive anthropogenic activities was the main contributor to the elevated sedimentary TOC contents.
The δ13C composition of organic matter in marine ecosystems was controlled by several factors, including the source of organic matter, changes in community structure of phytoplankton and productivity, and the input of dissolved inorganic carbon into the ocean (Meyers, 1994; Yu et al., 2012; Finkenbinder et al., 2015). Our results indicate a significant seaward increase in δ13C when comparing δ13C at the inshore station (Core C4) with that in the offshore stations (Cores C3, C5 and C6) (One-Way ANOVA, P<0.01). According to the previous study, the seaward increase in δ13C of marine sediment might be related to the seaward increase in marine photosynthetic organic matter relative to terrigenous organic matter (Gao et al., 2012). However, there was a significant seaward decrease in δ13C when δ13C at Stas C3 and C5 was compared with that in C6. The high δ13C at Stas C3 and C5 might have resulted from CO2 limitation due to eutrophication and high primary production of phytoplankton (Voβ and Struck, 1997; Ke et al., 2017). In the inner area of the Jiaozhou Bay, we did not find a typical riverine δ13C signal (i.e., depleted δ13C with value being less than 24.3‰). Actually, the Jiaozhou Bay is a typical eutrophic bay, where blooms frequently occur (Yuan et al., 2016), which can increase δ13C (Ke et al., 2017). Moreover, it was reasonable that the riverine TOC was partly diluted by the in situ produced TOC (Zhu et al., 2014). And hence there was no typical depleted δ13C in the inner bay. In addition, the surface partial pressure of carbon dioxide in the Jiaozhou Bay was below atmospheric partial pressure of carbon dioxide (Zhang et al., 2012), which indicated that the input of watershed respiration products had no effect on δ13C of dissolved inorganic carbon into the Jiaozhou Bay (Finkenbinder et al., 2015). Furthermore, the community structure of phytoplankton has changed obviously in the Jiaozhou Bay since 1954 (Wu et al., 2005), which can also influence the δ13C value (Yu et al., 2012).
The δ15N variation could reflect the change of productivity, the source of organic matter and the isotopic composition of the nitrogen input into the sea water (Yang et al., 2011; Yu et al., 2012; Wang et al., 2013). Our results indicate that δ15N in the inner bay (Cores C3 and C4) was significantly higher than that in the bay mouth (Core C5) (One-Way ANOVA, P<0.01). The lower δ15N in the bay mouth might be explained by a lower input of δ15N-enriched sewage and organism manure (Ruiz-Fernández et al., 2002; Cao et al., 2015; Ke et al., 2017). In addition, there was no significant correlation between TOC/TN ratio and δ13C in Core C5, whereas significant correlations were observed between the TOC/TN ratio and δ15N, and between δ13C and δ15N (P<0.05) (Table 1). It was because the diagenesis or anthropogenic disturbances might modify the organic composition in this area (Teranes and Bernasconi, 2000; Gao et al., 2012; Yu et al., 2012; Li et al., 2015a, b). The anthropogenic disturbances might be a more probable reason, which would be further proved by the δ15N data. More significantly enriched δ15N in Cores C3, C4 and C5 than in C6 were observed after 1942 (One-Way ANOVA, P<0.01), which might be related to the increased input of δ15N-depleted nitrogen fertilizers and ammonia in the industrial waste water or other factors.
The element and stable isotope composition of sediment samples in this study were summarized and compared with those of other marginal seas and bays (Fig. 5). The majority of sediment samples collected from these areas display intermediate TOC/TN ratios between 6 and 16 and relatively enriched δ13C signatures between –20.0‰ and –24.0‰ (Fig. 5), suggesting that organic matter may be originated from the mixture of various sources (Hu et al., 2016). The average TOC/TN ratio in the Jiaozhou Bay (11.48) was much higher than that in marginal seas, such as the Bohai Sea (8.33) (Liu et al., 2015), the Yellow Sea (7.99) (Hu et al., 2013) and the inner shelf of the East China Sea (7.14) (Li et al., 2015a; Hu et al., 2012) (Fig. 5). The TOC/TN ratio was also higher than that in those areas with obvious anthropogenic loadings, such as the Sishili Bay (9.36) (Wang et al., 2013) and the Gulf of Mexico (7.13) (Goñi et al., 1998), owing to the increasing TOC contents in the Jiaozhou Bay (Fig. 3). However, it should be mentioned that although the discharge of sediments from small rivers around the Jiaozhou Bay was relatively lower than those large rivers (e.g., the Changjiang River, the Huanghe River), the observed δ13C values in this area were more in line with a partly marine signature and comparable with those of other marginal seas and bays summarized in Fig. 5.
3.4 Environmental responses to anthropogenic activities and climate changes in the Jiaozhou Bay
Previous studies indicated that the anthropogenic activities including fertilizer use, sewage discharge, shipment, mariculture and deforestation had an obvious influence on the distribution of TOC, TN and its isotopic composition (Shen et al., 2005; Wang et al., 2013). With the reform and opening up of China since 1978, various anthropogenic activities (e.g., shipment, mariculture, sewage discharge, ammonia discharge and fertilizer use) have been performed dramatically around the Jiaozhou Bay, resulting in an increase in population and gross domestic production (GDP) (Figs 6a-h). The increase of population, Qingdao Port throughput, fishery and mariculture brought large amounts of industrial, agricultural and domestic sewage into the Jiaozhou Bay (Figs 6a-h). Although the data of the sewage discharge were not available before 1999, we speculated that the sewage discharge increased significantly with population increase. Our data suggest that the sewage discharge in 2015 increases to be 2.6 times that in 1999 (Fig. 6g). The discharge of ammonia into the bay was about 15.0 kt during 2015 (Fig. 6f). Moreover, with the rapid development of agriculture and fishery, large amounts of fertilizers were used for fast growth of plants and animals. The application of nitrogen fertilizers in 2015 increases to be 152 times that in 1957 (Fig. 6h).
All of the above changes were recorded by the geochemical proxies in the Jiaozhou Bay. For example, TOC and TN contents have presented an increasing trend with time in Cores C3, C4 and C5 since 1923, 1919 and 2003, respectively, implying the Jiaozhou Bay has been suffering from a heavy eutrophication since that time. However, after a statistical analysis, it could be concluded that the increase of TOC and TN contents in Cores C3 and C4 was not significantly influenced by a single anthropogenic activity (P>0.05). We speculated that the increase of TOC and TN contents in Cores C3 and C4 was the result of combined impacts from various anthropogenic activities and climate changes. The correlation analysis (r=0.77, P<0.05) indicates that the increase of TOC contents in Core C5 is significantly influenced by the ammonia discharge. Moreover, a significant positive correlation (r=0.74, P<0.05) of terrigenous TOC with sewage discharge amount, ammonia discharge amount (r=0.80, P<0.05) and Qingdao Port throughput (r=0.77, P<0.05) was observed in this area, indicating that the increase of TOC contents should be related to these anthropogenic activities, while the increase of TN contents was significantly influenced by the ammonia discharge amount (r=0.78, P<0.05) and the sewage discharge amount (r=0.74, P<0.05). In addition, a significant positive correlation (P<0.01) between TOC and TN and a negative correlation (P<0.01) between TOC and δ15N (P<0.01) suggested that the increasing TOC content was induced, at least partly, by the acute nitrogen pollution in the inner bay and the mouth of the bay. Although the impact of the anthropogenic activities on sediments in the outside bay (Core C6) was not significant (P>0.05), the sedimentary environment in this area has also changed since 1916. For example, the increase of terrigenous TOC content was significantly influenced by the increase of fertilizer utilization (r=0.74, P<0.05). Moreover, the impact of the anthropogenic activities on the burial flux of TOC was complex. For example, there was a significant positive correlation of the burial flux of TOC with fertilizer utilization in Core C3 (r=0.67, P<0.05) and a significant negative correlation of the burial flux of TOC with fertilizer utilization (r=–0.89, P<0.05) in Core C5. However, the burial flux of TOC content in Cores C4 and C6 was not significantly influenced by a single anthropogenic activity. That was because the burial flux of TOC was mainly influenced by the TOC concentration, the sedimentation rate and the sediment porosity (Li et al., 2008).
Similarly, the anthropogenic activities also exerted a significant influence on the isotope composition of δ13C and δ15N. For example, fertilizer utilization produced a significant influence on δ13C. The statistical analysis indicates that there is a significant negative correlation of δ13C with fertilizer utilization in Cores C3 (r=–0.66, P<0.05), C4 (r=–0.90, P<0.05), C5 (r=–0.65, P<0.05) and C6 (r=–0.85, P<0.05). That is because with the increase of fertilizer utilization, the terrigenous TOC content increased and consequently results in the low δ13C value. In addition, the δ13C in Core C5 is significantly influenced by sewage discharge amount (r=–0.78, P<0.05), ammonia discharge amount (r=–0.76, P<0.05) and Qingdao Port throughput (r=–0.87, P<0.05). That is because this area is influenced by the intensified anthropogenic activities from Qingdao City and Huangdao City. Moreover, the Qingdao Port is also located in this area. Previous studies indicate that δ15N can be influenced by the sewage discharge and fertilizer utilization (Ruiz-Fernández et al., 2002; Zhu et al., 2014). However, after the statistical analysis we found that the variation of δ15N in the Jiaozhou Bay was not significantly influenced by the sewage discharge and nitrogen fertilizer utilization (P>0.05). That is not to say the sewage discharge and nitrogen fertilizer utilization have no influence on the δ15N variation. The increase of the δ15N values with time in Cores C4 and C5 since the 1980s might be a result of various anthropogenic activities. The high δ15N (ranging from 9.7‰ to 17.6‰) in Core C4 during 1726–1941 might be related to the discharge of sewage (10‰ to 20‰) and the human or animal manure (7‰ to 25‰) (Ruiz-Fernández et al., 2002; Cao et al., 2015). However, δ15N in Cores C3 and C6 has decreased since 1923 and 1916, respectively, which is because the less effects of the sewage discharge on Cores C3 and C6 than Cores C4 and C5.
Climate changes can be better recorded by geochemical proxies including TOC, TN, TOC/TN ratios and δ13C (Shen et al., 2005, 2006; Li et al., 2015a; Rao et al., 2017). In this study, as the most important climatic factor, rainfall was used for the discussion of the impact of climate changes on environment changes. Rainfall in Qingdao City decreased concurrently from 792 mm during 1950–1976 to 642 mm during 1977–2015 (Fig. 7). Rao et al. (2017) indicate that there is a significant negative correlation between rainfall and the δ13C value. However, the significant negative correlation of δ13C with rainfall was only observed in Core C5 (r=–0.48, P<0.05). That might be because of the dam construction having weakened the influence of rainfall on the inner bay. In addition, the correlation analysis indicates that there is no significant correlation of TOC content, burial flux of TOC, terrigenous TOC content, TN content and δ15N with rainfall (P>0.05). The most likely reasons for weak statistical linkages between our proxies and rainfall are the multitude of other anthropogenic changes (e.g., river discharge, dam construction) that have occurred in the Jiaozhou Bay. Moreover, sectioning precision and possible errors of core chronology also contributed to these weak statistical linkages (Li et al., 2015a).
4 Conclusions
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Sedimentary organic carbon and nitrogen including isotopes are effective for historical trend reconstruction. In this study, TOC, TN and their isotope composition in four sediment cores were used to reflect the historical environmental changes in the Jiaozhou Bay on a centennial time scale. The increase of TOC and TN contents in Cores C3 and C4 since the 1920s was the result of combined impacts from various anthropogenic activities and climate changes, which indicated the probable eutrophication in the inner bay. The δ13C was significantly influenced by the fertilizer utilization. The δ15N might be influenced by sewage discharge and fertilizer utilization. In addition, the influence of rainfall on the isotopic composition of carbon and nitrogen in the inner bay was little. The increase of TOC and TN content in Core C5 since the 2000s was the result of ammonia and sewage discharge, which indicated the probable eutrophication in the mouth of the bay. The δ13C in Core C5 was significantly influenced by the fertilizer utilization, ammonia and sewage discharge, the Qingdao Port throughput and rainfall. The δ15N variation in Core C5 might be the result of various anthropogenic activities. The variation of terrigenous input in Core C6 suggested that the environments of the outside bay also have changed since 1916. The δ13C in Core C6 was significantly influenced by the fertilizer utilization, while the δ15N might be related to the sewage discharge or other anthropogenic activities. The source analysis indicates that organic matter of the Jiaozhou Bay is a mixture of terrigenous and marine sources. The results of two end-member δ13C isotopic mixing model indicate the organic matter is mainly from the marine source in the Jiaozhou Bay. The increased terrigenous TOC content illustrated an increased terrigenous loading and was associated to anthropogenic activities. As mentioned above, the environmental changes of the Jiaozhou Bay are the complex results of both anthropogenic activities and climate changes. There is much work to do to quantitatively discriminate the impacts from anthropogenic activities and climate changes in the near future.
Acknowledgements
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The authors thank Chen Min for providing the sediment rate data of Core C4. They also thank the colleagues in Key Laboratory of Marine Ecology and Environmental Sciences of Institute of Oceanology for their assistance in sample collection.
Funding
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  • The Joint Fund between Natural Science Foundation of China and Shandong Province under contract No. U1606404; the National Basic Research Program (973 Program) of China under contract Nos 2015CB452901 and 2015CB452902; the National Key Research and Development Plan Sino-Australian Centre for Healthy Coasts under contract No. 2016YFE0101500; the Program for Aoshan Excellent Scholars of Qingdao National Laboratory for Marine Science and Technology of China under contract No. 2015ASTP-OS13.
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Appendix
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Year 2017 volume 36 Issue 11
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doi: 10.1007/s13131-017-1076-1
  • Receive Date：2017-01-12
  • Online Date：2026-04-16
  • Published：2017-11-01
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  • Received：2017-01-12
  • Accepted：2017-02-08
Funding
The Joint Fund between Natural Science Foundation of China and Shandong Province under contract No. U1606404; the National Basic Research Program (973 Program) of China under contract Nos 2015CB452901 and 2015CB452902; the National Key Research and Development Plan Sino-Australian Centre for Healthy Coasts under contract No. 2016YFE0101500; the Program for Aoshan Excellent Scholars of Qingdao National Laboratory for Marine Science and Technology of China under contract No. 2015ASTP-OS13.
Affiliations
    1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
    2 Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
    3 University of Chinese Academy of Sciences, Beijing 100049, China

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*E-mail: (J. Song)
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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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