Abstract
Increasing attention has recently been drawn to oxygen depletion and ocean acidification in coastal seas and their impacts on the marine ecosystem. Intensive organic matter degradation combined with weak water exchange is considered to be mainly responsible for bottom water oxygen depletion and acidification. Hypoxia and acidification in the bottom water of Bohai Sea have been frequently observed in summer seasons over the past decade. In this study, monthly surveys were conducted along an inshore-offshore transect in the north Bohai Sea from May to August in 2017 and 2018. The physical structure of the water column in the study area was characterized by a well-mixed surface layer and an essentially homogeneous deep layer that were separated by a strong pycnocline over the period from mid-Jun to late August in both years. Dissolved oxygen (DO), pH, and dissolved inorganic carbon (DIC) in the water column were also split into two layers by the pycnocline and varied little in each layer. No significant interannual variations were observed for the temporal progressions of DO, pH and DIC in the bottom water. Average DO concentration and pH in the bottom water linearly decreased with time from May to August while DIC presented an opposite trend. DO became increasingly unsaturated from mid-June to late August when DO decreased to 96 μmol L–1 and pH to 7.74. The molar ratio of net oxygen consumption to DIC production was 1.42, similar to the Redfield ratio (1.30). Pelagic respiration (>60%) linked to degradation of fresh organic matter prevailed over sediment respiration (<40%) in contributing to the oxygen depletion and acidification observed in this shallow water body. The duration and intensity of oxygen depletion and acidification in the study area were strongly affected by stormy weather events such as typhoons.
Introduction
Water masses undergoing oxygen depletion and acidification are expanding globally in both open oceans and coastal seas (; ). Oxygen depletion and ocean acidification can reduce the ocean’s biodiversity (; ) and influence the abundance and activity of bacteria (; ). Prolonged exposure to low oxygen conditions may change the population and community structure of zooplankton () and benthic organisms (). Ocean acidification can also inhibit the activity of calcifying organisms (; ) and hence decrease the downward flux of CaCO3 to the deep ocean (). Consequently, oxygen depletion and ocean acidification have potentially important impacts on the structure and function of the marine ecosystem (), the ocean’s fisheries industry (; ), and the dynamics of organic and inorganic matter ().
Oxygen depletion and concomitant acidification in the bottom water of coastal seas stem from a combination of strengthened bacterial respiration and restricted water exchange (; ). The increase in bacterial respiration is often linked to eutrophication which enhances primary production () and therefore downward particulate organic matter transport to the bottom water and sediments. The relative contributions of pelagic and sedimentary respiration of organic matter to the water column oxygen consumption vary substantially among different hypoxic waters, depending to a large extent on the depth of the water column and the topography of the seabed (; ; ). Similarly, the relative contributions of fresh, autochthonous organic matter and old, allochthonous organic matter to the water column oxygen consumption differ considerably as well from one hypoxic system to another, depending in part on the quantity and lability of the allochthonous organic matter (; ; , ). In addition to organic matter input, stormy weather conditions, such as typhoons and hurricanes, can also strongly impact the duration and intensity of oxygen depletion and acidification in coastal bottom waters, given that these events can dramatically alter the physical stability of the water column and redistribute nutrients therein (; ; ).
Located in the northeast China, the Bohai Sea is a semi-closed coastal sea that is connected to the Yellow Sea to the east via the Bohai Channel (Figure 1). Eutrophication in the Bohai Sea has been deteriorating in the past 30 years due to industrialization and urbanization along its coast (; ) combined with its limited water exchange with the outside. Increasing eutrophication and strong water column stratification in summer have led to decreasing summertime dissolved oxygen (DO) concentration in the bottom water of the Bohai Sea in the past decades (; ). first reported the occurrence of significant oxygen depletion and acidification in the nearshore bottom water of the northeastern and northern Bohai Sea, with pH and DO decreasing by 0.29 and 170 μmol kg–1, respectively, from June to August. Later studies demonstrated that summertime oxygen depletion in the Bohai Sea shows a two-core feature corresponding to the two cold cores located in the bottom water of the western and northern Bohai Sea (; ). Currently, little is known about the duration, intensity, and interannual variability of the summertime oxygen depletion and acidification in the Bohai Sea. Moreover, the source (pelagic vs. sedimentary) and nature (fresh vs. old) of the organic matter dominating oxygen consumption in the bottom water of the Bohai Sea remain unclear, though organic matter degradation has been considered to be responsible for the observed oxygen depletion and acidification there (; ; ). In this study, we investigated the temporal evolution of DO, pH, and dissolved inorganic carbon (DIC) in the bottom water on the west coast of the Bohai Sea over two summer seasons to assess the rates of oxygen consumption and acidification and the pelagic vs. sedimentary contribution to the observed oxygen depletion and acidification. We also assessed the impact of Typhoon Rumbia, which passed over the Bohai Sea during late summer of 2018, on bottom water oxygen depletion and acidification in the study area.
FIGURE 1
TABLE 1
| Sampling dates (YD) | |||||
| 2017 | 2018 | ||||
| Station | Lat. (°N) | Long. (°E) | Water depth (m) | ||
| A3 | 39.618 | 119.840 | 21 | 178, 203, 234 | 162, 200, 220, 237 |
| A4 | 39.548 | 120.046 | 25 | 144, 178, 203, 234 | 162, 200, 220, 237 |
| A5 | 39.478 | 120.252 | 27 | 144, 178, 203, 234 | 162, 200, 220, 237 |
| A6 | 39.408 | 120.458 | 23 | 144, 178, 203, 234 | 162, 200, 220, 237 |
| A7 | 39.377 | 120.551 | 23 | NA | 162, 200, 220, 237 |
Coordinates, water depth, and sampling dates.
YD, day of the year; NA, samples were not collected.
Sample Collection and Analysis
DO, pH, and DIC were investigated during the summers of 2017 and 2018 along an inshore-offshore transect across the known oxygen depletion area with four cruises being conducted each year (Figure 1 and Table 1). The transect, located off Qinhuangdao City, crossed the southwest of the bowl-shaped depression extending from northeast to southwest (Figure 1;
After the collection of the water samples, current velocity at station A5 was continuously recorded for 47 h with a Nortek Acoustic Doppler Velocimetry (ADV) from 22:00 of day of year 220 (YD 220) in 2018. The downward-looking ADV sampling volume was set up at ∼0.3 m above the bottom, with a sampling rate of 32 Hz. Continuous temperature, salinity and DO concentration in this layer were determined by the RBR maestro multi-parameter. The mean downward oxygen flux through the bottom boundary layer (i.e., oxygen consumption by sedimentary organic matter, FBBL) at the interval of 0.5 h was calculated using Equation (1) (
where D is the oxygen diffusion coefficient (m2 s–1), CBBL is the DO concentration in the bottom boundary layer (μmol L–1), T denotes the temperature in the bottom boundary layer and Tm the mean temperature of the dataset during the continuous measurement. could be calculated based on the measured current velocity according to
Meanwhile, the turbulent kinetic energy (TKE) dissipation rate (ε) was hourly scanned using a vertical microstructure profiler (VMP-200) manufactured by Rockland Scientific International (RSI). The VMP was equipped with two high-frequency shear probes with a sampling frequency of 512 Hz. The TKE dissipation rate ε was estimated by fitting the empirical Nasmyth spectrum to the measured shear spectra with the calculation methods have been clearly depicted before (
where Γ (unitless) is the mixing efficiency and is assigned to be a constant of 0.2 (
where Δz stands for the thickness of the pycnocline and ΔDO for the difference in DO concentration between the upper and lower boundary of the pycnocline. ΔDO/Δz thus denotes the vertical gradient of DO across the pycnocline.
Results and Discussion
Physical and Biological Settings
The water depth along the transect ranged from 21 to 27 m, with the maximum occurring at station A5 (Table 1). The depth ranges of the pycnoclines, where N2 exceeded 0.001 s–2, at the sampling stations are shown in Table 2. Note that the pycnocline was undetectable, per the criterium of N2 >0.001 s–2, across the entire transect on YD 144 (24 May) in 2017 and at station A3 on YD 237 (25 August) in 2018, though weak stratification was visually noticeable on both occasions based on the vertical profiles of water temperature, salinity, and density (Figure 2). The absence of a fully developed pycnocline on YD 144(2017) was due to the relatively low surface water temperature (14.5–16.2°C) preventing the formation of a strong stratification. The passage of Typhoon Rumbia over the Bohai Sea on YD 231-232(2018), which created intensive turbulence, was mainly responsible for the weak stratification on YD 237(2018). Owning to the abrupt heavy wind just within 15 h before sampling on YD 203(2017), the depths of the pycnocline were much deeper than that during other cruises (Figure 2 and Table 2). During the other cruises, the water column was separated into a well-mixed surface layer (“surface layer” hereafter) and a nearly homogenous deep layer (“bottom layer” hereafter) by a strong thermocline or pycnocline (Figure 2 and Supplementary Figures S1, S2). In each layer, the water temperature and salinity (and thus density) varied little. Despite the lack of a quantifiable pycnocline, a bottom layer with depth > 16 m was assigned to YD 144(2017) based on the visually observable decrease in temperature and increase in density at the middle of the water column (14–16 m) (Figure 2). The vertical profile of temperature almost mirrored that of density, indicating that temperature was the dominant factor controlling the distribution of density. In contrast, the halocline was much weaker and the bottom-surface difference in salinity was mostly <0.87 across the entire transect. The lower-than-expected surface salinity on YD 200(2018) was due to the heavy precipitation in July. Water temperature generally increased with time in the whole water column. Yet surface water temperature along the entire transect on YD 237(2018) was 1.60 ± 0.94°C lower than that on YD 220(2018) due to the strong water column mixing by Typhoon Rumbia. Salinity slightly decreased from May to August in both years but the decrease was larger in 2018 because of a relatively heavier precipitation in 2018. As expected from the temporal trends of temperature and salinity, density gradually decreased from May to August in both years.
TABLE 2
| Sampling date | Range of pycnocline (m) | ||||
| A3 | A4 | A5 | A6 | A7 | |
| 2017 | |||||
| YD 144b | NAa | – | – | – | NA |
| YD 178 | 6–9 | 7–9 | 7–10 | 5–8 | NA |
| YD 203 | 13–17 | 11–17 | 12–18 | 13–15 | NA |
| YD 234 | 12–14 | 11–13 | 12–14 | 9–10 | NA |
| 2018 | |||||
| YD 162 | 7–10 | 12–14 | 12–15 | 12–13 | 7–11 |
| YD 200 | 8–9 | 8–10 | 8–9 | 7–9 | 8–9 |
| YD 220 | 11–13 | 12–16 | 10–14 | 9–11 | 8–13 |
| YD 237b | – | 20–21 | 15–18 | 9–11 | 7–9 |
Depth range of the pycnocline based on the buoyance frequency (N2).
aStation A3 on YD 144(2017) and station A7 in 2017 were not visited (see Table 1). bNo significant pycnoclines detected at stations A4–A6 on YD 144(2017), and at station A3 on YD 237(2018), based on the N2 values.
FIGURE 2

Vertical profiles of temperature (A,D), salinity (B,E), and density (C,F) for each cruise at station A5 in 2017 (upper panels) and 2018 (lower panels).
Vertical Profiles of DO, pHT, and DIC
The vertical profiles of DO, pHT, and DIC displayed a double-layer feature similar to that of density, i.e., homogeneous or weak gradients in the surface and bottom layers and rapid changes within the pycnoclines (Figures 3). DO and pHT in the surface layer were higher than in the bottom layer while DIC exhibited an inverse pattern. The temporal variations in pHT, DO, and DIC in the surface layer were generally less regular and smaller than those in the bottom layer. These phenomena can be attributed to more complex processes in controlling the dynamics of pHT, DO, and DIC in the surface layer (e.g., air-sea exchange, photosynthesis, respiration) than those in the bottom layer (mainly respiration only). In 2017, pHT and DO decreased while DIC increased progressively in the bottom layer from late May (YD 144) to late August (YD 234) (Figures 3A–C). In 2018, a similar temporal trend was seen in the bottom layer from mid-June (YD 162) to early August (YD 220) but this trend was sharply reversed in late August (YD 237) (Figures 3D–F) as a result of the disruption of the stable vertical structure of the water column by Typhoon Rumbia (Figure 2F).
FIGURE 3

Vertical profiles of DO (A,D), pHT (B,E), and DIC (C,F) for each cruise at station A5 in 2017 (upper panels) and 2018 (lower panels).
Oxygen Depletion and Acidification in the Bottom Layer
Since the water mass was essentially homogenous beneath the pycnocline (Supplementary Figures S1, S2), the average values of DO, pHT, and DIC in bottom water (see section Physical and Biological Settings) along the entire transect were calculated for discussion. For each sampling year, DO, pHT, and DIC changed linearly with YD (Table 3). Student’s t-test did not show significant interannual variations for the progressions of DO, pHT and DIC over the sampling periods (p > 0.45). The daily decreasing rates of DO and pHT obtained from the present study, i.e., the regressed slopes in Table 3, were also comparable with those in summer 2011 (DO: 2.13 ± 0.14 μmol L–1 d–1; pHT: 0.0038 ± 0.0006 d–1) observed near our sampling transect (
TABLE 3
| Parameter | Function | R2 | p |
| 2017 | |||
| DO | Y = (-2.25 ± 0.20)X + (631.5 ± 38.7) | 0.984 | <0.01 |
| pHT | Y = (-0.0037 ± 0.0006)X + (8.63 ± 0.12) | 0.944 | 0.03 |
| DIC | Y = (1.60 ± 0.37)X + (2051.9 ± 64.8) | 0.919 | 0.04 |
| 2018 | |||
| DO | Y = (-2.03 ± 0.14)X + (601.7 ± 27.0) | 0.995 | 0.02 |
| pHT | Y = (-0.0039 ± 0.0001)X + (8.67 ± 0.01) | 0.999 | <0.01 |
| DIC | Y = (1.41 ± 0.40)X + (2079.5 ± 78.5) | 0.925 | 0.18 |
Results of linear regression of the mean DO, pHT, and DIC in bottom water against day of the year (YD) performed separately for 2017 and 2018.
YD 237(2018) was excluded due to the influence of Typhoon Rumbia.
FIGURE 4

Temporal evolution of the mean DO (A), pHT(B), and DIC (C) in bottom water along the sampling transect. YD stands for day of the year. Error bars are 1 standard deviation. The solid and dashed lines are the linear fit to the data and 95% confidence interval, respectively. The solid blue points on YD 237 were excluded for data fitting.
TABLE 4
| Parameter | Function | R2 | p |
| DO | Y = (-2.18 ± 0.15)X + (622.2 ± 29.5) | 0.976 | <0.0001 |
| pHT | Y = (-0.0037 ± 0.0002)X + (8.64 ± 0.05) | 0.965 | <0.0001 |
| DIC | Y = (1.54 ± 0.22)X + (2060.4 ± 42.3) | 0.909 | <0.001 |
Results of linear regression of the mean values of DO, pHT, and DIC in bottom water against day of the year (YD) based on the composite data of 2017 and 2018.
YD 237(2018) was excluded due to the influence of Typhoon Rumbia.
Based on the regression of DO saturation degree against YD (Figure 5 and Table 4), DO in the bottom water switched from oversaturation to undersaturation on YD 164 (June 13), decreasing gradually from 264.7 ± 38.4 μmol L–1 to 90.3 ± 8.1 μmol L–1, or by 66% ± 17% over a period of ∼80 days from YD 164. Simultaneously, pHT progressively decreased from 8.03 ± 0.06 to 7.74 ± 0.07, or by 0.29 ± 0.09. The extent of oxygen depletion in our study area is comparable to those in the Gulf of St. Lawrence (
FIGURE 5

Temporal evolution of the mean DO saturation degree in bottom water. YD stands for day of the year. Error bars are 1 standard deviation. The solid and dashed lines are the linear fit to the data and 95% confidence interval, respectively. The solid blue point was excluded for data fitting. The regressed equation is: Y = (-0.67 ± 0.06) X + (210.0 ± 12.0), R2 = 0.96, p = 0.001.
Note that the data for YD 237(2018) was not included for the regression analysis shown in Figure 4 and Table 4 due to the influence of Typhoon Rumbia. The passage of the typhoon over the sampling area on YD 231-232(2018) greatly weakened the pycnocline, leading to enhanced vertical mixing of DO and DIC. Horizontal exchange with adjacent waters richer in DO but poorer in DIC might also be increased due to the elevated turbulence. Consequently, DO and pHT in bottom water on YD 237(2018) were 46.7 μmol L–1 and 0.17 higher and DIC was 159.5 μmol L–1 lower than expected from the fit to the data excluding YD 237(2018) (Figure 4 and Table 4). This result also indicates that the typhoon effect persisted at least to the end of our sampling campaign, ∼5 days after the typhoon event. Previous studies have demonstrated that typhoons could terminate bottom water oxygen depletion in the estuaries of the Yangtze River and Pearl River (
Pelagic vs. Sediment Oxygen Consumption
The oxygen diffusion flux through the pycnocline (i.e., the diapycnal diffusion flux) derived from Equation (3) for station A5 on YD 220–222(2018) ranged from 0 to 0.93 mmol m–2 d–1 and averaged 0.19 ± 0.21 mmol m–2 d–1 (Figure 6A). The concurrently determined oxygen flux at the water-sediment boundary layer, i.e., the sediment oxygen consumption rate, ranged from 0.27 to 10.26 mmol m–2 d–1 and averaged 6.32 ± 2.44 mmol m–2 d–1 (Figure 6B), which is comparable to that in the Oregen continental shelf (3.2–9.8 mmol m–2 d–1) (
FIGURE 6

Estimated DO fluxes at station A5 through the pycnocline (Fp) (A) and through the bottom boundary layer (FBBL) (B) as a function of time.
TABLE 5
| Cruise | Temperature (°C) | Salinity | DO (μ mol L–1) | D (×10–9 m2 s–1) | FBBL (mmol m–2 d–1) | Contribution (%) |
| 2017 | ||||||
| YD 144 | 10.8 | 32.21 | 311.6 | 1.505 | 11.25 | NA |
| YD 178 | 15.2 | 32.23 | 216.0 | 1.713 | 8.87 | 22.3 |
| YD 203 | 20.3 | 32.02 | 193.5 | 1.909 | 8.86 | 42.1 |
| YD 234 | 20.7 | 31.87 | 84.3 | 2.011 | 4.07 | 13.4 |
| 2018 | ||||||
| YD 162 | 9.4 | 32.73 | 286.1 | 1.417 | 9.72 | 34.6 |
| YD 200 | 12.7 | 32.32 | 212.0 | 1.588 | 8.07 | 19.2 |
| YD 220 | 16.9 | 31.98 | 145.7 | 1.809 | 6.32 | 20.8 |
| YD 237 | 22.7 | 31.29 | 158.0 | 2.103 | 7.97 | 37.8 |
Estimated DO fluxes through the bottom boundary layer (FBBL) and their contributions to the net oxygen consumption rate in bottom water at station A5, along with other parameters in the bottom water.
D, the oxygen diffusion coefficient; NA, not available.
The molar ratio of oxygen consumption to DIC production in the bottom water (O2/DIC hereafter) was calculated to be 1.42 ± 0.22 based on the slopes of the fitted DO vs. YD and DIC vs. YD equations (Table 4). This ratio is statistically indifferent from the Redfield ratio (1.30), suggesting that microbial oxidation of particulate organic matter freshly produced by marine plankton (e.g., phytodetritus) dominated oxygen consumption, as has been observed in the Gulf of Mexico (
Summary and Conclusion
Oxygen depletion of ∼90 μmol L–1 and acidification of ∼0.3 pH unit occurred in the bottom water of the Bohai Sea off Qinhuangdao City during the summers of 2017 and 2018. Combined with literature data, no significant interannual variations were observed in the rates of oxygen depletion and acidification from 2011 to 2018. The bottom water had therefore remained in a stable condition in terms of net community respiration over that period. The ratio of oxygen consumption to DIC production in the bottom water (1.42 ± 0.22) was close to the Redfield ratio (1.30), demonstrating that degradation of freshly produced organic matter dominated oxygen consumption. Sedimentary organic matter degradation contributed <40% of the oxygen depletion and acidification in the overlying bottom water. The passage of Typhoon Rumbia over the Bohai Sea in the late summer of 2018 strongly weakened the bottom water oxygen depletion and acidification. This study demonstrates that pelagic respiration can thus prevail over sediment respiration in generating oxygen depletion and acidification in shallow coastal systems and stormy weather events can substantially alter the duration and intensity of oxygen depletion and acidification in coastal areas.
Statements
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation, to any qualified researcher.
Author contributions
GS, LZ, FC, and HX designed the project. GS, LZ, and FL collected and analyzed the water samples. GS, LZ, and ML processed the data. GS and HX prepared the manuscript with input from all other authors.
Funding
This study was financially supported by the Natural Key Research and Development Program of China (2016YFC1401602), National Natural Science Foundation of China (41606098, 41876018, and 41806018), and Tianjin Natural Science Foundation (19JCZDJC40600 and 16JCQNJC08000). GS held a visiting scholarship (QNHX1811) at Second Institute of Oceanography, Ministry of Natural Resources during this study.
Acknowledgments
We thank W. Zhai for providing the 2011 DO and pH data, our colleagues for their help with the sample collection, and the crews for their cooperation during the cruises.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2020.00252/full#supplementary-material
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Summary
Keywords
oxygen depletion, acidification, dissolved inorganic carbon, organic matter degradation, typhoon, Bohai Sea
Citation
Song G, Zhao L, Chai F, Liu F, Li M and Xie H (2020) Summertime Oxygen Depletion and Acidification in Bohai Sea, China. Front. Mar. Sci. 7:252. doi: 10.3389/fmars.2020.00252
Received
26 February 2020
Accepted
30 March 2020
Published
24 April 2020
Volume
7 - 2020
Edited by
Xianghui Guo, Xiamen University, China
Reviewed by
Yuanyuan Xu, University of Miami, United States; Guoxiang Wu, Ocean University of China, China
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Copyright
© 2020 Song, Zhao, Chai, Liu, Li and Xie.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Guisheng Song, guisheng.song@tju.edu.cnHuixiang Xie, huixiang_xie@uqar.ca
This article was submitted to Coastal Ocean Processes, a section of the journal Frontiers in Marine Science
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