Science of the Total Environment 741 (2020) 140434

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

Occurrence and spatial distribution of organophosphorus ﬂame
retardants and plasticizers in the Bohai, Yellow and East China seas
Mingyu Zhong a, Jianhui Tang b,c,⁎, Xinyu Guo d, Chao Guo b,e, Fei Li b, Huifeng Wu ba

Ocean School, Yantai University, Yantai 264005, China
Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences, Yantai 264003, China
Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, ChinadCenter for Marine Environmental Studies, Ehime University, Matsuyama 790-8577, Japane
University of Chinese Academy of Sciences, Beijing 100049, Chinabc

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• OPEs were wildly detected in the Bohai(BS), Yellow (YS), and East China Seas
(ECS).
• OPE inventories were calculated in theBS, YS, and ECS.
• Ocean currents and riverine inputs inﬂuence the horizontal distributionof OPEs.
• River input and water stratiﬁcation inﬂuence the vertical distribution of OPEs.
• OPEs showed higher concentrations in
winter than in summer in the BS andthe YS.

a r t i c l e

i n f oArticle history:
Received 14 February 2020
Received in revised form 16 June 2020
Accepted 20 June 2020
Available online 23 June 2020
Editor: Jay Gan
Keywords:
Organophosphate esters
Concentrations and distributions
Seasonal variation
Chinese marginal sea

a b s t r a c t
Organophosphate esters (OPEs) are man-made organic pollutants that are used in ﬂame retardants (FRs), plasticizers, antifoaming and hydraulic agents, and extractants. The demand for FRs in China has increased, thereby
rapidly increasing the use of OPEs and hence resulted in its high levels in the environment. In this study, we measured the concentrations of seven OPE congeners in the seawaters of the Bohai Sea (BS), the Yellow Sea (YS), andthe East China Sea (ECS). The horizontal and vertical spatial distributions were then analyzed to assess the OPE
pollution. The total concentrations of the seven OPE congeners (ΣOPEs) in the three seas ranged from 7.31 to
100 ng L−1. The main OPE compounds were tris-(1-chloro-2-propyl) phosphate (TCPP, 3.97–35.6 ng L−1), tris(2-chloroethyl) phosphate (TCEP, 0.59–19.8 ng L−1), and triphenylphosphine oxide (TPPO, from below the detection limit to 43.5 ng L−1). The inventory of the ΣOPEs in the BS, YS, and ECS was estimated as 54.2, 513, and3950 tons, respectively. Horizontally, the ΣOPE concentration was ranked as BS N YS N ECS. In the vertical direction, the OPE concentrations in the surface water were higher than those in the bottom water. Ocean currents andriverine inputs might be the main factors inﬂuencing the distributions of the OPEs in these seas. Moreover, a seasonal variation (summer 2015 versus winter 2016) in the OPEs was observed in the YS, which was probably due
to anthropogenic inﬂuences and hydrological, meteorological, and biological factors.
© 2020 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of
Sciences, Yantai 264003, China.
E-mail address: jhtang@yic.ac.cn (J. Tang).

https://doi.org/10.1016/j.scitotenv.2020.140434
0048-9697/© 2020 Elsevier B.V. All rights reserved.

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M. Zhong et al. / Science of the Total Environment 741 (2020) 140434

1. Introduction
Organophosphate esters (OPEs) are man-made organic pollutants
with a central phosphorus atom and various substituent functionalgroups, according to which OPEs can be classiﬁed as alkyl, aryl, or chlorinated OPEs (Zhong et al., 2017; Zhong et al., 2018). In addition to theirmain used as ﬂame retardants (FRs), OPEs can also be used as plasticizers, antifoaming and hydraulic agents, and extractants in other industries (Reemtsma et al., 2008). OPEs were replaced by other ﬂame
retardants during the 1960s and 1970s owing to their signiﬁcant residual concentrations in the environment (Hao et al., 2018). However, withthe phasing out of certain polybrominated diphenyl ethers (PBDEs) by
the European Union's in 2004, OPEs, as ﬂame retardants, returned to
the global market as an efﬁcient alternative to PBDEs (Hao et al.,2018). The production and use of OPEs subsequently increased signiﬁcantly (Wang et al., 2015). In the western European market, the annual
consumption of OPEs increased to 80,000 tons (t), which accounted for
20% of the total FR market share at that time (Rodil et al., 2005). Meanwhile, as the largest developing country and the second largest economy worldwide, China had a demand for FRs of 300,000 t in 2013,
after which the country's usage of OPEs increased rapidly (Zhang,2014). Globally, approximately 500,000 t of OPEs was used in 2011,
and the market demand for OPEs was previously projected to reach
680,000 t by 2015 (Ou, 2011; van der Veen and de Boer, 2012).
OPEs are a type of additive ﬂame retardant, suggesting that they
non-covalently bond to the added materials and are liable to leachinto the environment (Zhong et al., 2018). These compounds, especiallythose that are chlorinated, are resistant to degradation after they enter
into the environment; therefore, it is difﬁcult to eliminate them fromthe environment. In recent years, several studies have investigated theoccurrence of OPEs in air (Fromme et al., 2014; Moller et al., 2012;
Staaf and Ostman, 2005), dust (Ali et al., 2012; Marklund et al., 2003;
Stapleton et al., 2009; Pang et al., 2019), water (Hu et al., 2014; Wanget al., 2015; Zhong et al., 2017; Niu et al., 2019), sediment (Cao et al.,2017; Wang et al., 2017; Zhong et al., 2018; Li et al., 2019), soil
(Mihajlovic et al., 2011), and biota (Chen et al., 2012; Liu et al., 2018;
Ma et al., 2013). The ﬁndings of these studies implied a ubiquitous existence of OPEs in the environment. Additionally, OPEs have been detected in remote areas far from the pollution sources, including theopen oceans (Li et al., 2017; Ma et al., 2017) and polar regions (Liet al., 2017; Sühring et al., 2016), which indicates their ability to undergo long-range transport (LRT). Although the toxicities of OPEs tohumans have not been reported sufﬁciently, their carcinogenicity, neurotoxicity, teratogenicity, cytotoxicity, and metabolic toxicity to otherspecies and human cells have been investigated in recent years, withthe ﬁndings suggesting the potential risks of OPEs to human health(Greaves and Letcher, 2017; Niu et al., 2019).
The Bohai Sea (BS), Yellow Sea (YS), and East China Sea (ECS) are
important marginal seas of China. These seas are adjacent to the mostdeveloped and populated regions in eastern China, and thereby receiving large volumes of domestic sewage and industrial wastewater, whichsigniﬁcantly deteriorate the coastal water quality (Hu et al., 2011; Ma
et al., 2001; Shen et al., 2013; Zhong et al., 2017). High concentrationsof OPEs have been detected in the BS and YS and in rivers draining
into these seas (Wang et al., 2015; Zhong et al., 2017). Meanwhile, theBS, YS, and ECS have complex hydrodynamic features, and the distributions of organic pollutants are profoundly inﬂuenced by ocean currents.
These currents include the Bohai Sea Coastal Current (BSCC), Subei
Coastal Current, Changjiang Diluted Water (CDW), Zhejiang Fujian
Coastal Current (ZFCC), Taiwan Warm Current (TaWC), and Yellow
Sea Warm Current (YSWC) (Liu et al., 2007; Zhong et al., 2017). However, the concentrations and distributions of OPEs in the seawater ofthe ECS and the seasonal variations (summer v.s. winter) of OPEs inthe seawater of the BS and YS have not yet been systematically studied
and discussed. Accordingly, this study collected and analyzed seawater
samples from 61 sites in the BS, YS, and ECS to (i) investigate theconcentrations, compositions, and distributions of 7 OPEs congeners[tris-(2-chloroethyl) phosphate (TCEP), tris-(1-chloro-2-propyl) phosphate (TCPP), tris-(1,3-dichloro-2-propyl) phosphate (TDCPP), triisobutyl phosphate (TiBP), tri-n-butyl phosphate (TnBP), triphenyl
phosphate (TPhP), and triphenylphosphine oxide (TPPO)]; (ii) explore
the factors that may inﬂuence the spatial distributions of these OPEs;and (iii) discuss the seasonal variations of these OPEs in the BS and YS.
2. Materials and methods
2.1. Sampling cruise
From November 10 to December 24, 2016 (i.e. winter), 177 seawater
samples from 61 sites in the Bohai Sea, Yellow Sea, and East China Sea
were collected during a cruise on the research vessel (Beidou) for the
analysis of OPE congeners (Table S1). The locations of the samplingsites are shown in Fig. 1 and are listed in Table S2. To reveal the verticalvariations of the seven OPEs, we collected seawater samples from thesurface and bottom layers in shallow water regions and from up to six
layers in deep water regions (Table S2). An automated conductivitytemperature-depth system (CTD) sampling device (Seabird 25, USA)equipped with Niskin bottles was used to collect the seawater samples
from the different layers.
2.2. Chemicals
All the organic solvents used in this study were of chromatographic
grade and were purchased from Merck (Germany). Information
concerning the analytical standards is provided in Table S1.
2.3. Sample pretreatment
The pretreatment process followed the procedure proposed by
Zhong et al. (2017) with minor modiﬁcations. In detail, 20 ng each ofsurrogates (D27-TnBP, D12-TCEP, and D15-TPhP) was added to 1 L seawater (for each sample), which was then ﬁltered through a glass microﬁber ﬁlter (pore size: 0.7 μm; Whatman, UK). The ﬁltered sample wasimmediately transferred to a pretreated separating funnel and passed
through an OASIS hydrophilic - lipophilic balance (HLB) cartridge(6 cm3, 200 mg; Waters) on board the R/V. The HLB cartridge waspretreated by adding 6 mL of ethyl acetate and 6 mL of methanol.
Then, it was sealed with cleaned foil and stored at −20 °C. Subsequently, the loaded HLB column was drained and eluted with 10 mLof ethyl acetate using solid phase extraction. Then, the eluent was frozen
overnight (at least 12 h) at −20 °C to remove water. The residual water
was removed again by adding 3 g of baked sodium sulfate. Then, the eluent was transferred to a new vial and evaporated to a volume of 200 μL
under a gentle nitrogen ﬂow. Finally, 20 ng of polychlorinated biphenyl
208 (PCB 208) was added before instrumental analysis as an injection
standard (see the Supporting Information).
2.4. Instrumental analysis
A gas chromatograph (Agilent 6890) coupled with a mass spectrometer (Agilent 5973) was employed to analyze all the pretreated samples,as described by Zhong et al. (2017). Details of the analysis processes areprovided in the Supporting Information.
2.5. Quality assurance and quality control
Both blank and spiked experiments were conducted to evaluate themethod blanks and recoveries, respectively. For the blank experiment,
40 ng each of surrogates (D27-TnBP, D12-TCEP, and D15-TPhP) was
added to 1 L of the ultra-pure water. For the spiked experiment, 40 ng
each of surrogates (D27-TnBP, D12-TCEP, and D15-TPhP) and 100 ng of
the seven OPE congeners were added to 1 L of the ultra-pure water.

M. Zhong et al. / Science of the Total Environment 741 (2020) 140434

3

Fig. 1. Water depth (color) and sample sites (marks). BS: Bohai Sea; YS: Yellow Sea; and ECS: the East China Sea. The arrows denote ocean currents for the Subei Coastal Water (SCW),
Changjiang Diluted Water (CDW), Yellow Sea Warm Current (YSWC), and Taiwan Warm Current (TaWC). The range of the sampling layers was from 1 to 2 m (surface layer) to 108 m(bottom layer), with detailed information provided in Table S2 of the Supporting Information. (For interpretation of the references to color in this ﬁgure legend, the reader is referredto the web version of this article.)

For both the blank and spiked experiments, 32 g of sodium chloride wasadded to the ultra-pure water for simulating the salinity of the seawater.
The remaining procedures were similar to those of the sample
pretreatment.
The concentrations of the method blanks ranged from 30 ± 25
(TnBP) to 433 ± 22 pg L−1 (TPPO) (n = 6), whereas the method recoveries ranged from 88% ± 2% (TPhP) to 107% ± 8% (TnBP) (n = 6). The
method detection limit (MDL) was deﬁned as the method blanks plus
three times the standard deviation (3σ) of the method blanks andranged from 82 (TPhP) to 529 pg L−1 (TPPO). Detailed information regarding the blanks, recoveries, MDL, and limit of instrumental detection(LOD) (calculated at a signal-to-noise ratio of 3) are listed in Table S1.
2.6. Statistical analysis
The OPE concentration data were extracted by Chemstation Data
Analysis software and further processed using Excel 2017. A signiﬁcanceanalysis between the data was performed using SPSS 19.0 one-way
analysis of variance (ANOVA) and paired sample t-test. The distributions of the OPE concentrations were plotted using ArcGIS 10.0.
3. Results and discussion
3.1. OPE concentrations
Overall, ﬁve of the seven OPEs (TCEP, TCPP, TDCPP, TPhP, and TPPO)
were detected in the seawaters of the Bohai Sea, Yellow Sea, and East
China Sea, whereas the remaining two OPEs (TiBP and TnBP) were
only sporadically detected in the BS and YS. The concentration data forthe seven OPEs are listed in Table S2 and summarized in Table 1. As
shown in Table 1, the total concentrations of the seven OPEs (ƩOPEs)
in all three seas ranged from 8.81 to 100 ng L−1, with a geometricmean concentration (GM) of 24.0 ng L−1. The ƩOPE concentrations
ranged from 19.7 to 100 ng L−1 (GM of 39.1 ng L−1) in the Bohai Sea,

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M. Zhong et al. / Science of the Total Environment 741 (2020) 140434

9.26 to 86.8 ng L−1 (GM of 30.7 ng L−1) in the Yellow Sea, and 8.81 to
55.7 ng L−1 (GM of 15.1 ng L−1) in the East China Sea.
Of the individual OPEs, the chlorinated OPEs (i.e., TCEP, TCPP, and
TDCPP) and TPPO were the main OPE compounds, whereas alkyl andaryl congeners only accounted for a small proportion of the total. As
shown in Table 1, the concentrations of TCEP and TCPP ranged from0.59 to 19.8 ng L−1 (GM of 4.04 ng L−1) and from 3.97 to 35.6 ng L−1(GM of 11.3 ng L−1), respectively, with 100% detection rates for both.
As another chlorinated OPE, the concentration of TDCPP (from b MDL
to 8.13 ng L−1; GM of 1.16 ng L−1) was signiﬁcantly lower (P b 0.01)
than the concentrations of the TCEP and TCPP. Meanwhile, the detection
rate of TDCPP was 89%, which was also lower than that of the TCEP and
TCPP. The concentration of TPPO ranged from b MDL to 43.5 ng L−1,
with a detection rate of ~100%. With respect to the two alkyl OPEs, theconcentrations of TiBP ranged from bMDL to 27.4 ng L−1 (GM of
0.166 ng L−1), whereas that of TnBP ranged from bMDL to 37.2 ng L−1(GM of bMDL). The detection rates of TiBP and TnBP only reached 24%
and 5%, respectively.
3.2. Calculation of the OPE inventories
As OPEs were frequently detected in the seawater of the Bohai Sea,
Yellow Sea and East China Sea, the inventories of the ƩOPEs and individual OPEs in these areas were calculated using the method proposed by
Cao et al. (2017). The average water depth of the BS, YS, and ECS is 18,
44, and 340 m, respectively, with each covering an approximate areaof 7.70 × 104, 3.80 × 105, and 7.7 × 105 km2, respectively. The estimatedvolume of seawater in the BS, YS, and ECS is 1.386 × 1012, 1.672 × 1013,
and 2.618 × 1014 m3, respectively. By multiplying the volume of seawater with the geometric mean concentrations of the ΣOPEs and individual
OPEs (Section 3.1 and Table 1) in each sea, the inventory of the OPEs ineach region was determined (Table 2). The inventory of the ƩOPEs
ranged from 54.2 t from the BS to 3953 t for the ECS, and TCPP in the
ECS was the most abundant individual OPE.
According to Ou (2011), the phasing out of BFRs in China led to ademand gap between 1.5 × 105 and 2.0 × 105 t in non-brominatedﬂame retardant such as OPEs, and the annual consumption growth of
OPEs was expected to reach 15%. Compared with the usage of OPEs in
China, input of the OPEs into the three marginal seas still only
accounted for a relatively small proportion. This suggested that the
OPEs had not entirely leached out from the added materials and/orthat a considerable proportion of the OPEs had not yet entered the marine environment.
3.3. Spatial distributions of the OPEs
3.3.1. Horizontal distribution of the OPEs
Fig. 2 shows that the Bohai Sea exhibited the highest ƩOPE concentrations, followed by the Yellow Sea and East China Sea. The horizontal
distributions of TiBP and TCEP concentrations followed the pattern ofthe ƩOPE concentrations. This can be explained by the fact that there
are more pollution sources around the Bohai Sea than those aroundthe Yellow Sea and the East China Sea, as well as the poorer water exchange in the Bohai Sea than that in the Yellow Sea and East China
Sea, which are closer to the western Paciﬁc Ocean) (Zhong et al.,2017). Meanwhile, TnBP was only detected at one site (B3) in the
Bohai Sea and sparsely detected at several sites in the Yellow Sea. Thisphenomenon might be attributed to the limited sources of this OPE in
the Bohai Sea and the Yellow Sea and its high degradability as an alkyl
OPE (Regnery and Puttmann, 2010). Interestingly, the distribution of
TnBP in the N1-N4 section showed an obvious decreasing trend fromthe south (Shandong Province) to the north (Liaoning Province),
which implies limited sources of TnBP in the Shandong Province.
The concentrations of TCPP, TDCPP, and TPPO exhibited different
distribution patterns than those of the ƩOPEs (Fig. 2). These three compounds presented higher concentrations in the Yellow Sea than in the

Bohai Sea and the East China Sea, which suggests that there was a higher
input of these OPEs in the Yellow Sea. In fact, one of the largest OPE
manufacturers in China is located on the west coast of the southern Yellow Sea, with an annual OPE production of 20,000 t and TCPP and TDCPP
being their dominant products. Meanwhile, dozens of pharmaceuticalcompanies are also situated in Jiangsu Province, and they use TPPO asintermediates for producing medicines. Thus, waste water from thesecompanies could be regarded as an exclusive TPPO source to the Yellow
Sea (Wang et al., 2015; Zhong et al., 2017). Interestingly, on the S11-S13
transect (Fig. 2), the concentrations of several individual OPEs (TDCPP,
TCPP, and TPPO) and the ƩOPEs were also higher at the sites adjacentto the Korean Peninsula side in comparison to sites in the middle ofthe transect. This pattern indicates that there might also be OPE sourceson the Korean Peninsula, and that the OPEs from these sources weretransported to site S13. This hypothesis was partially supported by thesurface currents, as shown in Fig. S1 in the Supporting Information. Nevertheless, with the ascending trends of salinity among the transects (E1E2, E3-E6, E7-E10, E11-E14, E15-E18 and E19-E20), the distribution of
the OPEs in the East China Sea agreed well with the descending trend
from the nearshore to the offshore regions, which is a typical pattern
for land sourced pollutants. However, site E16 on the E15-E18 transect
had higher OPE concentrations than those of the nearshore E15 site.
Meanwhile, relatively high OPE concentrations were found at the
Oujiang estuary (OE) site, which also suggests a terrigenous origin of
OPEs in the E15-E18 transect. Thus, it can be argued that this phenomenon may be due to the dilution of the OPE concentration at site E15
by the Taiwan Warm Current (TaWC, Fig. 1), which originates from abranch of the Kuroshio Current along with seawater inputs from thesoutheast of Taiwan (Wei et al., 2016; Zhong et al., 2017).
3.3.2. Vertical distribution of the OPEs
The vertical distribution of the seven OPEs in the three seas was also
obtained. As shown in Table S3, in comparison with the concentrations
in deeper layers, the surface water was characterized by a higher concentration of ƩOPE, TCEP, TCPP, and TPPO in the entire region(P b 0.05, n = 61). This was also observed for the Yellow Sea(P b 0.05, n = 26) and the East China Sea (P b 0.05, n = 20). Meanwhile,the bottom water exhibited a higher salinity (32.6‰) than that of thesurface water (32.2‰) in the whole region (P b 0.01), which was also
the case for the Yellow Sea (surface: 31.6‰ v.s. bottom: 32.0‰;
P b 0.01) and the East China Sea (surface: 33.4‰ v.s. bottom: 34.0‰;
P b 0.01) (Fig. S2). Vertically, the OPE concentrations were negatively
correlated with salinity, which indicates that the vertical distributionof the seven OPEs could mainly be attributed to riverine inputs into
the surface water and the dilution effect of high- salinity open ocean
water in the bottom layers (Zhong et al., 2017). This argument was partially veriﬁed by the huge differences in the ƩOPE concentrations andsalinity between the surface water and the bottom water at site E7,
which is located in the central region of the CDW (Figs. 1 and 2). The origin of the CDW is the Changjiang River, which is the largest riverdraining into the East China Sea and has been found to be characterizedby high pollutant concentrations and low salinity (Kwon et al., 2018).
The relatively high ƩOPE concentration (55.7 ng L−1) in association
with a low salinity (29.4‰, which was the lowest in the East China
Sea) of the surface water, and the relatively low ƩOPE concentration(26.5 ng L−1) in association with a high salinity (32.7‰) in the bottom
water at E7 site might have been due to the inﬂuence of the CDW. This isa typical example that show the dominant effects of riverine inputs on
the vertical distribution of OPEs.
Atmosphere deposition could be another factor affecting the vertical
distribution patterns of OPEs. Li et al. (2018) estimated the annual atmospheric dry deposition of OPEs into the Bohai and Yellow Seas tobe 12 t. The authors found that TCPP was the most abundant compounds, followed by TCEP, TiBP and TnBP. This input is comparable to
the riverine inputs estimated by Wang et al. (2015). Thus, the OPE
ﬂux from the atmosphere may have been a signiﬁcant additional source

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5

Table 1
Summary of OPE concentrations in the Bohai Sea (BS), Yellow Sea (YS), and East China Sea (ECS).
Regions

ValuesOPEs

GMs (ng L−1)
Max. (ng L−1)
Min. (ng L−1)
GMs (ng L−1)
Max. (ng L−1)
Min. (ng L−1)
GMs (ng L−1)
Max. (ng L−1)
Min. (ng L−1)
GMs (ng L−1)
Max. (ng L−1)
Min. (ng L−1)

BS

YS

ECS

Sum

TiBP

TnBP

TCEP

TCPP

TDCPP

TPhP

TPPO

ƩOPEs

6.96
27.4
1.97
bMDL
9.64
bMDL
bMDL
bMDL
bMDL
0.166
27.4
bMDL

bMDL
37.2
bMDL
bMDL
26.5
bMDL
bMDL
bMDL
bMDL
bMDL
37.2
bMDL

9.56
19.8
6.06
5.84
16.9
1.24
1.93
12.4
0.59
4.04
19.8
0.59

11.4
26.7
3.97
13.1
35.6
5.17
9.63
29.6
5.61
11.3
35.6
3.97

2.03
5.16
bMDL
2.07
8.13
bMDL
0.51
4.92
bMDL
1.16
8.13
bMDL

0.15
3.28
bMDL
0.14
0.76
bMDL
0.11
1.95
bMDL
0.13
3.28
bMDL

5.16
26.6
1.86
6.93
43.5
1.18
1.63
19.1
bMDL
3.64
43.5
bMDL

39.1
100
19.7
30.7
86.8
9.26
15.1
55.7
8.81
24.0
100
8.81

that resulted in high OPE concentrations in the surface water. However,
although the Bohai Sea also presented a higher salinity in the bottom
water than that in the surface water (P b 0.01), the OPE concentrationsin the bottom water were not signiﬁcantly lower than those of the surface water (P N 0.05). This phenomenon could be attributed to more pollution sources in the Bohai Sea, e.g., pollutant discharge zones andmarine landﬁll (Zhong et al., 2018), which might act as additionalsources for bottom water. Meanwhile, the shallow water depth (withan average depth of 18 m) of the Bohai Sea is prone to be well-mixedby big wave in winter, and might also disturb the vertical distribution
patterns of salinity and OPE concentrations.
In addition, the temperature difference between the surface waterand bottom water was also considered. The surface water only showeda higher average temperature (13.8 °C) than that of the bottom water(11.9 °C) in the Yellow Sea (P b 0.05, n = 26), which indicates thatthe relationship between the OPE concentrations and temperature
was not as obvious as that of salinity. The signiﬁcance of the surfacebottom water temperature difference may be attributed to the Yellow
Sea Cold Water Mass (YSCWM), which resides in the bottom of the Yellow Sea and is characterized by lower temperatures during the summer(Wei et al., 2016). According to Zhong et al. (2017), the YSCWM could
induce a water stratiﬁcation effect, thereby hindering the vertical exchange of the OPEs during the summer. Although this water mass begins to decline in the late autumn, it might still to some extent
inﬂuence the vertical distribution of OPEs during the winter to someextent.
Further, with an aim of investigating the vertical distribution of theseven OPEs in detail, additional sea water samples from different layers(surface, subsurface, middle, sub-bottom, and bottom) were collected atsites S9, S13, E14, and E18. As shown in Fig. 3, the concentrations ofƩOPEs and main individual OPEs (TCEP, TCPP, and TPPO) decreased
with the increasing water depth before increasing again in the subbottom and/or bottom layers at all four sites. The decrease in the OPE
concentrations from the surface to the middle layers could be attributed
to more OPE sources (e.g., riverine inputs and atmospheric deposition)in the surface water (Zhong et al., 2017), whereas the rebounded in theconcentrations below the middle layer can be attributed to an exchange
between the sediment and bottom water. According to Zhong et al.
(2018), sediment represents a reservoir of OPEs and might be a potential source to upper layer sea water. Moreover, OPEs residing in the
Table 2
Summary of OPE inventories for the BS, YS, and ECS.
Regions

BS
YS
ECS

Inventories of OPEs (ton)
TiBP

TnBP

TCEP

TCPP

TDCPP

TPhP

TPPO

ƩOPEs

9.65
–
–

–
–
–

13.3
97.6
505

15.8
219
2521

2.81
34.6
134

0.208
2.34
28.9

7.15
116
427

54.2
513
3953

bottom and sub-bottom water could hardly diffuse into the upper layers
due to thermoclines, as shown in Fig. 3, which usually formed below the
middle layers. Thermoclines act as barriers to the vertical movement of
the water and thus also for the OPEs dissolved within it, which could
also have contributed to the rebound in the OPE concentrations in the
sub-bottom and/or bottom water.

3.4. Seasonal variation of the OPEs in the Bohai Sea and the Yellow Sea
Seasonal variations have been observed for several pollutants, suchas polycyclic aromatic hydrocarbons (PAH) (Ya et al., 2017), acidvolatile sulﬁde (Li et al., 2016), and organophosphorus pesticide(Mamta et al., 2015). Herein, based on the OPE concentrations reported
by Zhong et al. (2017) and the data presented in the current study, we
examined the seasonal variation (summer 2015 v.s. winter 2016) of
OPE concentrations in the Bohai Sea and the Yellow Sea. During thesummer of 2015, the GM concentrations of the ƩOPEs (also TCEP,
TCPP, TDCPP, TnBP, TiBP, TPhP, and TPPO, i.e., the same as the present
study) in the Bohai Sea and the Yellow Sea were 33.4 and 21.0 ng L−1,
respectively, whereas those during the winter of 2016 were 39.1 and30.7 ng L−1, respectively. The seasonal variation in the ƩOPE concentrations was assessed using a one-way ANOVA, which revealed that there
was only a signiﬁcant difference between the data for the summer of2015 and winter of 2016 for the Yellow Sea (P b 0.01). The main individual OPE concentrations (i.e., TCEP, TCPP, and TPPO) also showed a similar seasonal variations as that showed by ƩOPE concentration, although
TCEP was an exception becausee the TCEP concentration during thesummer was not signiﬁcantly lower than that during the winter in the
Yellow Sea. According to Ya et al. (2017), the seasonal variation in organic pollutants may be primarily attributed to the combined effects
of multiple hydrological, meteorological, and biological factors,e.g., dilution by open-ocean water, surface runoff (mainly riverine inputs), atmospheric deposition, and biotic/abiotic enrichment and/or
degradation.
A one-way ANOVA was also used to compare the salinity between
the summer of 2015 and winter of 2016 to elucidate whether the seasonal variation in the OPEs was inﬂuenced by the dilution effects of
the YSWM. YSWM is a branched of the Kuroshio Current and is characterized by a relatively high salinity and low pollutant concentrations(Lian et al., 2016). However, the results showed that there was no statistical signiﬁcance between the salinity in the two seasons, and the GM
salinity in summer (31.0‰) was even lower than that in the winter(31.8‰). This implies that the dilution effects of open-ocean highsalinity seawater brought by the YSWM was not the dominant inﬂuencing factors for the OPE seasonal variation. Based on these results, we
propose that riverine inputs and atmosphere deposition could havebeen among the main factors inﬂuencing the seasonal variation of theOPEs; however, no detailed data regarding the seasonal variation in6

M. Zhong et al. / Science of the Total Environment 741 (2020) 140434

Fig. 2. Concentrations (average values of each layer at every site) and distribution patterns of the OPEs in the BS, YS, and ECS. OE: Oujiang estuary.

the rivers draining into the Yellow Sea or the atmospheric inputs to the
Yellow Sea have been reported to date.
Interestingly, although TiBP and TnBP were not the main OPE pollutants in this area, they did show obvious seasonal variations. During thesummer in the Bohai Sea, TiBP was only detected at a few sites with afairly low GM concentration of 0.45 ng L−1, whereas TiBP was ubiquitously detected during the winter with a GM concentration of
6.96 ng L−1. Similarly, in the Bohai Sea and the Yellow Sea, TnBP was undetectable during the summer; however, it was detected at several sites(B3, N1, N2, and N3) during the winter. The obvious seasonal variations
for these two alkyl OPEs may be attributed to the photolysis and biodegradation of non-halogenated OPEs (Regnery and Puttmann, 2010), and/or the additional large emissions related to their recent usage. Regnery
and Puttmann (2010) found that non-halogenated OPEs were liable tobe degraded in the presence of light and microorganism. The alkyl
OPEs (TiBP and TnBP) would have received less sunlight during the winter and would have also experienced relatively lower microorganism
degradation due to the lower temperatures in comparison with that inM. Zhong et al. / Science of the Total Environment 741 (2020) 140434

7

Fig. 3. Vertical distributions of the total OPEs (ƩOPEs) and the individual OPEs at sites S9 (A), S13 (B), E14 (C), and E18 (D).

summer. In the Bohai Sea and Yellow in our study, TiBP and TnBP may
have been subjected to alleviated photolysis and biodegradation effects,
thereby resulting in the higher concentrations in winter than those insummer. On the N1- N4 transect (from Shandong Province to Liaoning
Province), the TnBP concentration exhibited an obvious declining
trend and TnBP was undetectable at site N4. This pattern might indicatethat there were limited sources of TnBP in Shandong Province. Overall,
the seasonal variations of TiBP and TnBP reﬂect the combined effectsof photolysis, biodegradation and pollution sources.
4. Conclusion
This study analyzed the concentrations, distributions, and inventories of seven OPEs in the Bohai Sea, the Yellow Sea, and the East China
Sea. Seasonal variations of the OPEs in the Bohai Sea and the Yellow
Sea were compared. Relatively high concentrations of halogenatedOPEs (TCEP and TCPP) were observed, although TPPO was the main
OPE pollutant. The highest ƩOPE concentrations was found in the
Bohai Sea, followed by the Yellow Sea and East China Sea. Ocean currents and riverine inputs could be among the main factors that inﬂuencing the horizontal distribution of the OPEs, whereas riverine inputs andatmospheric deposition together with water stratiﬁcation may inﬂuence the vertical distribution of the OPEs in the study area. Inventory
calculations suggested that the seven OPEs dissolved in seawater only
accounted for small proportion in comparison with the amounts used.
With respected to seasonal variations of the seven OPEs, relatively
higher concentrations were determined during the winter that thosein the summer in the Bohai Sea and the Yellow Sea. The data obtainedin the present study shed light on the concentrations and distributionsof OPEs in the marginal seas of China, especially in the East China Sea,
and can help us to better monitor the pollution status of the OPEs. The
high concentrations of the OPEs found in some coastal regions during

8

M. Zhong et al. / Science of the Total Environment 741 (2020) 140434

this study, along with the extensively reported toxicities of OPEs to organisms and humans, highlight that more attention should be given to
the alleviation of OPE pollution.
CRediT authorship contribution statement
Mingyu Zhong:Investigation, Methodology, Software, Writing- original draft.Jianhui Tang:Conceptualization, Supervision, Writing review & editing, Data curation, Funding acquisition.Xinyu Guo:Visualization, Software, Validation.Chao Guo:Investigation, Writing - review& editing.Fei Li:Writing - review & editing.Huifeng Wu:Writing - review & editing, Supervision, Resources.

Declaration of competing interest
No conﬂict of interest exits in the submission of this manuscript. The
manuscript is approved by all authors for publication. I would like to declare on behalf of my co-authors that the work described was original
research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part. All the authors
listed have approved the manuscript that is enclosed.
Acknowledgement
This study was supported by the National Natural Science Foundation of China (No. 41773138 and U1806207), and by the project of Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences (No.
YIC Y855011024). Hydrological data were courtesy by Dr. Z.Y. Wang
from the Institute of Oceanology, Chinese Academy of Sciences, andare sincerely acknowledged. Special thanks to the crew of R/V ‘BEIDOU’for their generous helps.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2020.140434.
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