Science of the Total Environment 664 (2019) 522–535

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

A simulation of the seasonal variation of decabromodiphenyl ether in a
bay adjacent to the Yellow Sea
Aobo Wang a, Xinyu Guo a,b,⁎, Jie Shi a,c, Chongxin Luo a, Huiwang Gao a,cabcKey laboratory of Marine Environment and Ecology, Ocean University of China, Ministry of Education, 238 Songling Road, Qingdao 266100, China
Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo-Cho, Matsuyama 790-8577, Japan
Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T• We developed a three-dimensionaltransport-ecosystem-POP coupled model.
• We applied the coupled model to BDE209 in Jiaozhou Bay for the ﬁrst time.
• Concentrations of BDE-209 are higher insummer than in winter.
• River discharge and horizontal advection are important for mass balance ofBDE-209.
• Seasonal variation of BDE-209 is inﬂuenced by river discharge and watertemperature.

a r t i c l e

i n f oArticle history:
Received 8 November 2018
Received in revised form 31 December 2018
Accepted 28 January 2019
Available online 04 February 2019
Editor: Adrian Covaci
Keywords:
BDE-209
Jiaozhou Bay
Transport model
Seasonal variation
Mass balancea b s t r a c t
A three-dimensional transport-ecosystem-POP coupled model is conﬁgured to simulate the seasonal variation
and budget of decabromodiphenyl ether (BDE-209) in a semi-enclosed bay adjacent to the Yellow Sea. The
model includes ﬁve types of BDE-209 (gaseous, dissolved, phytoplankton-bound, detritus-bound, and suspended
particulate matter (SPM)-bound) and related physical and biogeochemical processes, such as advection anddiffusion due to seawater motion, input from rivers, air-sea exchange, decomposition of dissolved BDE-209,
uptake and depuration between dissolved and phytoplankton-bound BDE-209, mortality of phytoplanktonbound BDE-209, remineralization and sinking of detritus-bound BDE-209, and sinking of SPM-bound BDE-209.
Model results show that the dissolved and particulate BDE-209 in the bay are higher in the nearshore area
than in offshore area and are higher in summer than in other seasons; these results are consistent with ﬁeld
data. SPM-bound BDE-209 is dominant among the ﬁve types due to its large supplying from rivers. Dissolved
BDE-209 concentrations are around 5-fold that of phytoplankton-bound BDE-209, which depends on uptake
and depuration rate constants between dissolved and phytoplankton-bound BDE-209 and biomass of phytoplankton. Evaluation of mass balance indicates that the input from rivers is major source of BDE-209, while theexchange with the Yellow Sea is major sink. Sensitivity experiments demonstrate that the input of BDE-209
from rivers plays the most signiﬁcant role in the seasonal variation of dissolved and particulate BDE-209 concentrations, and the change in water temperature is a secondary factor.
© 2019 Elsevier B.V. All rights reserved.

1. Introduction⁎ Corresponding author at: Key laboratory of Marine Environment and Ecology, Ocean
University of China, Ministry of Education, 238 Songling Road, Qingdao 266100, China.
E-mail address: guoxinyu@sci.ehime-u.ac.jp (X. Guo).

https://doi.org/10.1016/j.scitotenv.2019.01.385
0048-9697/© 2019 Elsevier B.V. All rights reserved.

Persistent organic pollutants (POPs) are characterized by their persistence, high toxicity, long-range transport, and bioaccumulation,
which can be harmful to human health through food chains and webs

A. Wang et al. / Science of the Total Environment 664 (2019) 522–535(Zhong et al., 2014; Meng et al., 2017). Polychlorinated biphenyls(PCBs), polycyclic aromatic hydrocarbons (PAHs), and organochlorine
pesticides (OCPs) are traditional POPs, while polybrominated diphenyl
ethers (PBDEs) and perﬂuorinated compounds (PFCs) are relatively
new POPs (Ding et al., 2015; Meng et al., 2017).
The atmosphere and ocean are two of the primary media for longrange transport of POPs, and the ocean is considered to be one ofthe persistent organic pollutant (POP) reservoirs (Iwata et al., 1993;
Wania et al., 1998). POPs in the ocean come mainly from the atmosphere, rivers, and sediment. POPs in the atmosphere enter seawater
through three ways—dry deposition, wet deposition, and diffusive airsea exchange (Totten et al., 2001; Jurado et al., 2005, 2007). Amongthese three ways, diffusive air-sea exchange plays the most signiﬁcantrole in some regions and for some POPs (Totten et al., 2001; Jurado
et al., 2005). Diffusive air-sea exchange ﬂuxes of POPs can be calculatedusing a two-ﬁlm model (Bidleman and McConnell, 1995; Wania et al.,
1998; Dachs et al., 1999, 2002). The input of POPs from rivers has
been reported to be the dominant source of POPs in coastal waters(Ilyina et al., 2006, 2008; Zhong et al., 2014; Alekseenko et al., 2018).
Moreover, POPs in the sediment can return to the water column
through resuspension (Adeleye et al., 2016).
Since POPs are generally hydrophobic, dissolved POPs in seawater
are easily absorbed by phytoplankton and suspended particulate matters (SPM), which leads to the decrease in dissolved POP concentrationsin the water and, therefore, affects the diffusive air-sea exchange
ﬂuxes of POPs (Dachs et al., 1999; Gioia et al., 2012). Uptake rates ofPOPs by phytoplankton depend on water temperature, phytoplankton
biomass, and biochemical properties of target POPs. For example, thebioconcentration factor is a function of the octanol-water partition
coefﬁcient (Kow) of target POPs (Dachs et al., 1999, 2002; Del Vento
and Dachs, 2002). Natural degradation of POPs, although weak, is also
a process that affects POP concentration in seawater. The highly
brominated Decabromodiphenyl ether (BDE-209) decomposes throughdebromination and has different decomposition coefﬁcient in a variety
of media (Wania and Dugani, 2003; Bastos et al., 2009; Sun et al.,2009, 2012).
Due to heavy human activities, POPs are detected in atmosphere,
seawater, and sediment in Chinese coastal areas (Fu et al., 2007;
Pan et al., 2007; Jin et al., 2011; Gioia et al., 2012; Li et al., 2012; Duanet al., 2013; Zhong et al., 2014; Wang et al., 2015b, 2016; Ju et al.,2016). Concentrations and distributions of POPs in different areas
are different, which are inﬂuenced by pollution sources, transportconditions, and their biochemical properties (Zhong et al., 2014; Meng
et al., 2017).
Although there have been many reports on the POPs in the atmosphere, seawater, and sediment in the Chinese coastal areas, the understanding of their distribution remains at a qualitative discussion.
Understanding of their horizontal transport and temporal variations is
also lacking. Apparently, ﬁeld surveys and laboratory analysis are not
sufﬁcient to reveal the transport route of POPs; a numerical simulationis necessary for a quantitative understanding of POP transport andbudget.
The global POP model is an atmosphere-ocean-land coupled model,
which can simulate spatial distributions and temporal variations in
POPs in different media, i.e., air, ocean, and soil (Schenker et al., 2008;
Stemmler and Lammel, 2009, 2010; Guglielmo et al., 2009; Hansen
et al., 2015). However, the horizontal resolution of the global POP
model is usually low and, therefore, some process oriental POP models
and regional POP models have also been established. A box model wasused to simulate the exchange processes of POPs between air, seawater,
and phytoplankton (Dachs et al., 2002). Meijer et al. (2006, 2009)
applied the BIODEP model to a lake and indicated that the adsorption ofPOPs onto suspended particles may detain the POPs transporting from
air into water. Ilyina et al. (2006, 2008) applied a three-dimensional
FANTOM model in the North Sea to study the fate of POPs. However,their model did not incorporate biochemical processes of POPs, although523

these processes are important to POP concentrations in the water (Dachset al., 1999, 2002; Gioia et al., 2012; Meijer et al., 2006; Zhong et al., 2014).
Moreover, a three-dimensional transport-POP coupled model was usedin the East China Sea to simulate the seasonal variations of POPs and its
control factors (Ono et al., 2012). However, the phytoplankton concentrations in this model were based on satellite data (Ono et al., 2012; Uitz
et al., 2006). Recently, a three-dimensional hydrodynamic-ecosystemPOP coupled model was used to simulate transport of PCB153 in the
Gulf of Lions (Alekseenko et al., 2018).
As shown above, ocean transport models for POPs have gradually included realistic biogeochemical processes in POP transport simulation,with the purpose of reproducing the behavior of POPs in a marine environment. In this study, we also use a three-dimensional high-resolutionhydrodynamic-ecosystem-POP coupled model to reproduce the spatial
distribution and seasonal variation of POPs in a semi-enclosed bay,
Jiaozhou Bay, which is adjacent to the Yellow Sea and surrounded by
Qingdao city, an industrialized city in China. Decabromodiphenyl
ether (BDE-209), a widely used brominated ﬂame retardant (BFR),
which may cause endocrine disorders and affect generation oforganisms (Wahl et al., 2010; Ding et al., 2015), is chosen as the target
POP for simulation. One important reason to choose BDE-209 as a target
POP is that its observed values are available (Ju et al., 2016) and can beused to verify model results. After conﬁrming that our model can obtain
BDE-209 concentrations on the same order as observations (Ju et al.,2016), we conduct a budget calculation for the entire bay and quantify
the biogeochemical processes related to BDE-209.
2. Model description
A three-dimensional high-resolution transport-ecosystem-POP
coupled model is established to simulate the transport and biogeochemical processes of BDE-209 in Jiaozhou Bay. The model has threemodules: hydrodynamic module, low trophic ecosystem module, andPOP module. We use it to simulate the seasonal variation and spatial
distribution of BDE-209 in the bay and examine the mechanisms
responsible for its variation through sensitivity experiments.
2.1. Hydrodynamic and ecosystem modules
Contaminants in the seawater are transported by ocean currents
through advection and diffusion. The hydrodynamic module is athree-dimensional hydrodynamic model for Jiaozhou Bay (Cai et al.,2014), based on the Princeton Ocean Model (Mellor et al., 2002) andset for year 2005. The year 2005 is simulated because observational
data of BDE-209 are available for that year. The model domain is from
120.0795° E to 120.4271° E and from 35.9467° N to 36.2595° N(Fig. 1); it contains a grid interval of 0.0022° in the zonal direction and0.0017° in the meridional direction, and 5 sigma layers (0.00, −0.25,−0.50, −0.75, −1.00) in the vertical direction. To consider the tidal
land region, the hydrodynamic module has the capability of shiftingwetting and drying grids with a critical depth of 0.05 m. The hydrodynamic module is forced by wind, river discharges, heat ﬂuxes, four
major tidal constituents, and ocean current at the open boundary. The
atmospheric variables for calculating the heat ﬂux and wind stresses
in 2005 were downloaded from the European Center for Medium
Weather Forecasting (ECMWF, https://apps.ecmwf.int/datasets/data/interim-full-daily/levtype=sfc/). The open boundary conditions,
i.e., hourly water temperature, salinity, current velocities, and sea levelin 2005 were provided by the National Marine Environmental Forecasting Center (NMEFC). The open boundary data are interpolated from theresults of a large region model from the NMEFC (Ji et al., 2017a, 2017b).
The ecosystem module is coupled to the hydrodynamic module. The
ecological variables in the ecosystem module include phytoplankton,
detritus, dissolved oxygen, chemical oxygen demand, zooplankton,
nitrate, nitrite, ammonium, phosphate, and silicate (Liu et al., 2007).
The conceptual scheme of the ecosystem module is shown in Fig. 2.

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A. Wang et al. / Science of the Total Environment 664 (2019) 522–535

calculation and acts as a source of BDE-209 into the seawater throughthe air-sea exchange process. The equations for each state of BDE-209
in the seawater are as follows.


∂C w
∂C w
∂C w
∂C w
∂
∂C w
Kh
þu
þv
þw
¼
þ DðC w Þ þ SðC w Þ þ BioðC w Þ
∂z
∂t
∂x
∂y
∂z
∂z

ð1Þ



∂C wpm
∂C wpm
∂C wpm
∂C wpm
∂C wpm
∂
Kh
þu
þv
þw
¼
þ D C wpm
∂z
∂t
∂x
∂y
∂z
∂z

þ Bio C wpm

ð2Þ





∂C wps
∂C wps
∂C wps
∂C wps
∂C wps
∂
Kh
þu
þv
þw
¼
þ D C wps þ Bio C wps
∂z
∂t
∂x
∂y
∂z
∂z

ð3Þ

Fig. 1. Model domain and bathymetry (color tone). White dots are observation stations
where the biogeochemical variables are available for year 2005. Dashed line is locationof section for Fig. 6.

The ecosystem module supplies concentrations of chlorophyll a anddissolved oxygen, and the mortality rate of phytoplankton for POP
calculation. The forcing data of ecological variables in the ecosystemmodule, including nutrient concentrations in river water and surface
and bottom ﬂuxes of nutrients, are values averaged over several years
because observed values for 2005 are not available.
2.2. POP module
2.2.1. Transport equations for POPs
BDE-209 in the POP module has ﬁve states: dissolved BDE-209,
phytoplankton-bound BDE-209, detritus-bound BDE-209, SPM-boundBDE-209, and gaseous BDE-209. Their concentrations are expressed as
Cw, Cwp, Cwd, Cws, and Ca, respectively. Among them, Cwp is the sum of
BDE-209 adsorbed on phytoplankton surface (Cwps) and BDE-209
uptake in phytoplankton matrix (Cwpm), while Ca is speciﬁed before



∂C wd
∂C
∂C
∂C
∂
∂C
K h wd þ DðC wd Þ
þ u wd þ v wd þ ðw þ ws1 Þ wd ¼
∂z
∂t
∂x
∂y
∂z
∂z
þ BioðC wd Þ

ð4Þ



∂C ws
∂C ws
∂C ws
∂C ws
∂
∂C ws
Kh
þu
þv
þ ðw þ ws2 Þ¼
þ DðC ws Þ þ SðC ws Þ
∂z
∂t
∂x
∂y
∂z
∂z

ð5Þ
In these equations, t is the time (s); x, y, and z are the zonal, meridional, and vertical coordinates (m); u, v, and w are velocity components
in three directions (m s−1); ws1 and ws2 are sinking velocities (m s−1)of detritus and SPM, respectively, and their values are given in
Table A.1 in Supplementary material; Kh is vertical eddy diffusion coefﬁcient (m2 s−1); Cw, Cwps, Cwpm, Cwd, and Cws are BDE-209 concentrations(μg · m−3); D(Cw), D(Cwps), D(Cwpm), D(Cwd), and D(Cws) are horizontal
diffusion terms; S(C w ) and S(C ws ) are source terms; and Bio(C w ),Bio(C wps ), Bio(C wpm ), and Bio(C wd ) are biogeochemical terms.
S(Cw), S(Cws), Bio(Cw), Bio(Cwps), Bio(Cwpm), and Bio(Cwd) are describedin Appendix A in Supplementary material. The numerical scheme of
the POP calculation in the model is similar to the variables of the ecosystem module. Eqs. (1) to (5) are calculated by two steps: an explicit
scheme for horizontal and vertical advection, horizontal diffusion, andFig. 2. Conceptual scheme of the ecosystem module (Neumann, 2000; Liu et al., 2007). The ecosystem module includes following compartments: phytoplankton (PHY), zooplankton−+−
2−(ZOO), detritus (DET), dissolved oxygen (DO), chemical oxygen demand (COD), nitrate (NO−3 ), nitrite (NO2 ), ammonium (NO4 ), phosphate (PO4 ), silicate (SiO3 ), and nitrogen (N2).

A. Wang et al. / Science of the Total Environment 664 (2019) 522–535

the source and biogeochemical terms, and an implicit scheme forvertical diffusion.
2.2.2. Sources and biogeochemical processes of POPs
Fig. 3 shows a schematic of the transport and biogeochemical processes for the simulation of BDE-209 in Jiaozhou Bay. BDE-209 enters
the bay through air-sea diffusive exchange and river discharge; meanwhile, it leaves the bay through advection and diffusion at the bay
mouth, and sinking to the sea bottom with particles. Some dissolved
BDE-209 in seawater is decomposed due to light, while other BDE-209
is absorbed by phytoplankton through uptake and adsorption. The
uptake and adsorption of POPs by phytoplankton are reversible,
i.e., phytoplankton-bound POPs (Cwp) can return to dissolved POPs
through depuration and desorption. Phytoplankton-bound POPs become detritus-bound POPs (Cwd) through the mortality of phytoplankton. Some of the detritus-bound POPs are brought to the deep waterand sea bottom by the sinking of detritus, while other detritus-boundPOPs are transformed back to dissolved POPs through remineralizationof detritus. SPM-bound POPs in the model are assumed to be of terrigenous origin and, therefore, given from rivers. Theirs sinking velocity issmaller than detritus because they are generally smaller than detritus(Table A.1, Lima and Doney, 2004; Fennel et al., 2006). The calculations
for sources and biogeochemical processes of BDE-209 are described inAppendix A. The initial conditions and open boundary conditions forthe ﬁve types of BDE-209 variables are from ﬁeld data and are given
in Table 1 (Ju et al., 2016). The gaseous BDE-209 concentration in air isfrom data reported by Jin et al. (2011). The dissolved and SPM-boundBDE-209 concentrations in rivers are from data reported by Fu et al.
(2007), Chu et al. (2013), and Ju et al. (2016). The details of BDE-209
in air and rivers are given in Appendix A. The simulation time is 2 yr.
We used the results in the second year for our analysis to avoid theinﬂuence of initial conditions.
3. Results
3.1. Comparison with observations
Hydrodynamic variables, like temperature, salinity, and ﬂow
velocities have been compared with ﬁeld data, demonstrating that thehydrodynamic module is capable of reproducing the temporal-spatial
variabilities of the physical ﬁeld in Jiaozhou Bay (Cai et al., 2014). As
for ecological variables, we compared chlorophyll a (Chla), dissolved
oxygen (DO), chemical oxygen demand (COD), dissolved inorganic
nitrogen (DIN), dissolved inorganic phosphorus (DIP), and dissolved
silicon (DSI) with some available ﬁeld data and conﬁrmed that the525

Table 1
Initial and boundary conditions of BDE-209.
Concentration

Initial conditions

Open boundary conditions

Cw (μg · m−3)
Cwpm (μg · m−3)
Cwps (μg · m−3)
Cwd (μg · m−3)
Cws (μg · m−3)

1.0
0
0
0
4.0

0.2
0
0
0
2.0

Reference
Ju et al., 2016
Ju et al., 2016
Ju et al., 2016
Ju et al., 2016
Ju et al., 2016

ecosystem module can also capture the observed features of these
ecological variables. Because the POP module uses chlorophyll a anddissolved oxygen concentrations given by the ecosystem module, we
present a detailed comparison of these two ecological variables withﬁeld data obtained in 2005 (Sun and Sun, 2010) in Appendix B in
Supplementary material.
Particulate POPs in the model includes phytoplankton-bound POPs,
detritus-bound POPs, and SPM-bound POPs. Among these three typesof particulate POPs, phytoplankton-bound and detritus-bound POPs
are produced within seawater, while SPM-bound POPs are of terrigenous origin and enter seawater through rivers. Phytoplankton-boundand detritus-bound POPs are collectively referred to as biological POPsin this study and are denoted as Cwbio. They are important for the transport of POPs through the food chain to high trophic animals.
Seasonal variations of dissolved and particulate BDE-209 concentrations, including the SPM-bound and biological categories, averaged overthe entire Jiaozhou Bay, are shown in Fig. 4, in which the spatially averaged ﬁeld data are also presented (dots with same color as the lines).
Compared with ﬁeld data in February, the model outputs of dissolved
and particulate BDE-209 concentrations match with observations on
magnitude.
Although there are no data directly supporting it, the four forms of
BDE-209 are all highest in summer. Among them, the SPM-boundBDE-209 has a higher concentration than the dissolved BDE-209 while
the latter has a higher concentration than biological BDE-209. Observations for nonylphenol, a kind of POP, show a continuous increase in concentration from January to April to July in Jiaozhou Bay (Fu et al., 2007).
This is similar with model results of BDE-209. Differing from dissolved
and SPM-bound BDE-209, biological BDE-209 has the lowest concentration at the beginning of April, and the responsible reason is explained in
the next section.
Fig. 5 shows the horizontal distributions of dissolved and particulate
BDE-209 in Jiaozhou Bay. The available ﬁeld data for dissolved andparticulate BDE-209 in February 2005 are also presented in Fig. 5a & e.
The simulated BDE-209 concentrations at the nearshore area andFig. 3. Conceptual scheme of the coupled model for BDE-209 simulation (Dachs et al., 1999, 2002; Del Vento and Dachs, 2002; Ono et al., 2012). The POP module includes ﬁvecompartments: dissolved POPs (Cw), phytoplankton-bound POPs (Cwp), detritus-bound POPs (Cws), SPM-bound POPs (Cws), and gaseous POPs (Ca).

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runoff is the largest among the rivers surrounding the bay, is locatedin the northwestern area of the bay, and the estuary of the Moshui
River, which is seriously polluted (Fu et al., 2007), is in the northeasternarea of the bay. The BDE-209 load from the two rivers induces high concentrations of dissolved and SPM-bound BDE-209 in the areas close to
the two estuaries. The water exchange with the Yellow Sea throughthe open boundary leads to a low concentration at the bay mouth.
Fig. 6 shows vertical distribution of dissolved and particulate BDE209 along a section from nearshore areas to open bay (Fig. 1). Because
Jiaozhou Bay is shallow and the tidal currents are strong, it is a verticallyhomogenous bay, even in summer (Chen et al., 1999; Cai et al., 2014).
Therefore, the concentrations of dissolved and particulate BDE-209 are
also vertically homogeneous in the four seasons.
3.2. Temporal-spatial BDE-209 ﬂuxes of different processes evolution

Fig. 4. Time series of daily averaged dissolved, particulate, SPM-bound, and biological BDE209 concentrations averaged over entire Jiaozhou Bay while dots with same color are
corresponding spatially averaged ﬁeld data. Both simulation and observation are surface
data and the observation for the ﬁeld data is in February of 2005.

middle part of Jiaozhou Bay match well with ﬁeld data. However, theyshow a little difference at the bay mouth. There are harbors and someshipping routes near the bay mouth. The BDE-209 contaminant produced by ships is not considered in our calculations. If we compare thetwo types of BDE-209, both simulations and observations show alower concentration for dissolved BDE-209 than particulate BDE-209.
As a common feature in the four seasons, dissolved and particulate
BDE-209 concentrations are all high at the northeastern and northwestern areas of the bay and decrease gradually from the nearshore areas tooutside of the bay (Fig. 5). The estuary of Dagu River (Fig. 1), whose

Particulate BDE-209 includes phytoplankton-bound, detritus-bound,and SPM-bound BDE-209, in which only detritus-bound and SPMbound BDE-209 sink to the bottom in the model. Their bottom ﬂuxes
have an apparent seasonal variation: large in summer and small in
winter (Fig. 7). Their bottom ﬂuxes (Fig. 8c & d) have a similar horizontal
distribution with the particulate BDE-209 concentration (Fig. 5e–h):decreasing gradually from the nearshore area to offshore area.
Apparently, the concentration of particulate BDE-209 determines its
bottom sinking ﬂux.
Differing from the bottom ﬂux of BDE-209, the surface ﬂux of
BDE-209 is small (Fig. 7). In most months, the BDE-209 surface ﬂux
in Jiaozhou Bay is from air to sea (Fig. 7). However, its direction
reverses in August and September (Fig. 7). The surface ﬂux of BDE-209
has a slight horizontal variation in winter (Fig. 8a) but a large one insummer (Fig. 8b).
Magnitude and direction of the surface ﬂux are affected by watertemperature, wind speed, and concentration difference of BDE-209
between air and sea ( CHa0 −C w ). Here H′ is the dimensionless Henry's
law constant and the calculation of H′ is given in Appendix A. Low
water temperature, high wind speed, and large concentration difference
between air and sea are all favorable conditions for BDE-209 to enter thesea from air. In February, the direction of surface ﬂux is from air to sea,

Fig. 5. (a-d) Horizontal distributions of dissolved BDE-209 and (e-h) particulate BDE-209 concentrations in four months in Jiaozhou Bay. Dots with blank cycles represent values of ﬁeld
data. Both simulation and observation are surface data and the observation for the ﬁeld data is in February of 2005.

A. Wang et al. / Science of the Total Environment 664 (2019) 522–535

527

Fig. 6. (a-d) Vertical distributions of dissolved BDE-209 and (e-h) particulate BDE-209 concentrations along the section shown by dashed line in Fig. 1.

and the ﬂux value is relatively large in the area with lower temperature(Cai et al., 2014) and lower dissolved BDE-209 concentrations (Fig. 8a).
In August, the value and direction of surface ﬂux vary largely (Fig. 8b).
The air-sea ﬂux is still from air to sea in the offshore area but reverses
from sea to air in the nearshore area. Such an abrupt change is caused
mainly by the high dissolved BDE-209 concentration (Fig. 5c) in thenearshore area, which turns the concentration difference between airand sea negative and, therefore, the ﬂux direction reverses. The highwater temperature in the nearshore area (Cai et al., 2014) should also
contribute to this reversal because it affects the value of H′.
In addition to the sea surface and bottom, there are two other interfaces in which the BDE-209 ﬂux exits. A large source of BDE-209 is fromrivers, and a large sink is export to the Yellow Sea (Fig. 9). The BDE-209
ﬂux from rivers includes dissolved BDE-209 and SPM-bound BDE-209,
both of which have a large value in summer (Fig. 9b & c). Amongthese two types of BDE-209, the SPM-bound one has a larger ﬂux thanthe dissolved one.
At the lateral boundary with the Yellow Sea, the BDE-209 ﬂux isalways negative (Fig. 9a & d), indicating that BDE-209 is removed
from Jiaozhou Bay to the Yellow Sea by advection and diffusion. The

BDE-209 ﬂux through the lateral boundary with the Yellow Sea is thesame order of magnitude as that from the rivers. It also exhibits a similarseasonal variation as that from rivers, but its peak appears with a time
lag of one month compared with that from rivers. Notably, the magnitude of the BDE-209 ﬂuxes from rivers and through the lateral boundarywith the Yellow Sea are larger than the BDE-209 ﬂuxes through the sea
surface and bottom (Fig. 7), by one order of magnitude.
The one month lag between peaks of BDE-209 ﬂux from rivers andthat through the lateral boundary with the Yellow Sea is caused by
the physical and biogeochemical processes inside the bay. It has beenreported that groundwater requires one month to reach the mouth of
the bay (Wang et al., 2015a); calculation using the same hydrodynamic
model shows that the Dagu river water has an age of 30–45 days at themouth of the bay (Sun et al., 2018). Therefore, the one month of lag
between the two BDE ﬂuxes is consistent with these timescales.
The biogeochemical processes of BDE-209 inside the bay include net
absorption (= difference between uptake and depuration) by phytoplankton, mortality of phytoplankton, and remineralization of detritus(Fig. 3). The ﬂuxes of BDE-209 related to these processes in the bay arehigher in August and September than in the other months (Fig. 10),

Fig. 7. Time series of surface and bottom ﬂux of BDE-209 in Jiaozhou Bay. Positive surface ﬂux means that the BDE-209 is from air to sea while negative surface ﬂux is inverse; positive
bottom ﬂux means that BDE-209 is from sea to sediment. Black dashed line represents the value equal to zero.

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A. Wang et al. / Science of the Total Environment 664 (2019) 522–535

Fig. 8. Horizontal distributions of (a, b) simulated surface ﬂux and (c, d) bottom ﬂux of BDE-209 in (a, c) February and (b, d) August. Positive surface ﬂux indicates that the direction of airsea exchange is from air to sea while negative surface ﬂux is related to inverse air-sea exchange direction; positive bottom ﬂux means that BDE-209 is from sea to sediment.

maintaining a good relationship with the seasonal variation in the concentrations of dissolved and biological BDE-209 (Fig. 4). Magnitudes of
BDE-209 mortality and remineralization ﬂuxes are approximately
equal to each other, which results in the extremely low detritus-boundBDE-209 concentration in Jiaozhou Bay (Fig. 10). When the net absorption ﬂux is larger than the remineralization ﬂux, the biological BDE-209
concentrations increase and vice versa. For example, the net absorption
ﬂux minus the remineralization ﬂux is close to zero and lower than the
biological BDE-209 ﬂux at the lateral boundary with the Yellow Sea atthe beginning of April (Fig. 9d), which caused a low biological BDE-209
concentration (Fig. 4).
The net absorption ﬂux of BDE-209 to phytoplankton is inﬂuenced
by uptake, depuration, adsorption, desorption constants, biomassof phytoplankton, and dissolved and phytoplankton-bound BDE-209
concentrations (Eqs. (A.11)–(A.12) in Supplementary material).
Depuration, adsorption, and desorption constants have a positive
relation and the uptake constant has a negative relation to watertemperature (Del Vento and Dachs, 2002). Consequently, the transfer
rate of dissolved BDE-209 to the phytoplankton phase BDE-209 depends not only on the concentrations of the two phases of BDE-209
but also on water temperature (Del Vento and Dachs, 2002). A highdissolved BDE-209 concentration is favorable to its transfer to thephytoplankton-bound BDE-209; meanwhile, a high water temperature
is favorable to the adsorption of BDE-209 by phytoplankton but adverse
to uptake.
As shown in Fig. 11a, the net absorption ﬂux to phytoplankton in
February is higher in the nearshore area than in other areas, which is
caused by higher dissolved BDE-209 concentration in the nearshore
area than in the other areas (Fig. 5a). However, the net absorption ﬂux

to phytoplankton in February is lower in the middle of the bay thanoutside the bay, which is not consistent with distribution of dissolved
BDE-209 concentration (Fig. 5a). Therefore, the higher water temperature outside the bay must be reason for the large net absorption ﬂux
there (Fig. 11a). In August, the net absorption ﬂux to phytoplankton ishigher in estuarine areas than in other areas. This is caused by theextremely high dissolved BDE-209 concentrations in estuarine areas(Fig. 5c). However, the net absorption ﬂux is not always consistent
with the dissolved BDE-209 concentration in August because there is anegative net absorption ﬂux at the bay mouth where the water temperature and biomass of phytoplankton are all higher than those outside
the bay. In August, higher water temperature prevents the uptake of
dissolved BDE-209 to phytoplankton but promotes the adsorption.
Because the uptake is stronger than adsorption, the net absorption
ﬂux is lower at the bay mouth than outside the bay.
Biological BDE-209, which is signiﬁcant for BDE-209 transport in thefood web, includes phytoplankton-bound and detritus-bound in themodel, while detritus-bound BDE-209 concentrations are very low
due to the extremely high remineralization ﬂux. As a result, biologicalBDE-209 concentrations mainly depend on the phytoplankton-boundBDE-209 concentrations, which are inﬂuenced by biomass of phytoplankton and the ability of BDE-209 to be absorbed by phytoplankton.
Phytoplankton concentrations are around 100 mgC m−3 converted
from chlorophyll a concentrations (Fig. B.1 in Supplementary material)using a ratio of 50 mgC m−3/mgChl. a m−3 (Liu et al., 2007). Uptake (ku),depuration (kd), adsorption (ksu), and desorption (ksd) constants of
BDE-209 at 25 °C are 2200 m3 kg−1 day−1, 1.49 day−1, 115,000 m3
kg−1 day−1, and 287.6 day−1 (Dachs et al., 1999), respectively.
Consequently, when the uptake and adsorption reach equilibrium

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529

Fig. 9. (a) Time series of BDE-209 ﬂux discharge from rivers and BDE-209 ﬂux through open boundaries. Negative open boundary ﬂux indicates that BDE-209 is delivered from the bay by
advection and diffusion, and positive open boundary ﬂux is related to inverse exchange direction. Red-dashed line is averaged BDE-209 ﬂux through open boundaries among ﬁfteen days.
(b) Time series of dissolved BDE-209 ﬂux discharge from each river. (c) Time series of SPM-bound BDE-209 ﬂux discharge from each river. (d) Time series of dissolved, SPM-boundand biological BDE-209 ﬂux through open boundaries, averaged among ﬁfteen days. Negative open boundary ﬂux indicates that BDE-209 is delivered from the bay by advection anddiffusion and positive open boundary ﬂux is related to inverse exchange direction. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web
version of this article.)

Fig. 10. Time series of daily integrated net absorption ﬂux of dissolved BDE-209 by phytoplankton, phytoplankton-bound BDE-209 ﬂux through mortality of phytoplankton, and detritusbound BDE-209 ﬂux though remineralization of detritus in Jiaozhou Bay. Net absorption ﬂux refers to ﬂux of (uptake-depuration) + (adsorption-desorption).

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A. Wang et al. / Science of the Total Environment 664 (2019) 522–535

Fig. 11. Horizontal distributions of simulated biogeochemical ﬂux of BDE-209, including (a, b) net absorption, (c, d) mortality, and (e, f) remineralization processes; in (a, c, e) February and(b, d, f) August.

(Fcwpm (Eq. (A.11)) and Fcwps (Eq. (A.12)) equal to 0) at 25 °C, Cw : Cwpm
and Cw : Cwps reach critical values in the reversible absorption process,which are 6.6 and 25, respectively. As a result, the critical value of Cw :(Cwpm + Cwps) would be approximately equal to 5.2 in summer (watertemperature at around 25 °C), and Cw : (Cwpm + Cwps + Cwd) would
be similar to Cw : (Cwpm + Cwps). In other words, Cw : Cwbio would approximately be equal to 5.2 in summer when uptake and adsorptionof BDE-209 by phytoplankton reach equilibrium, which is indicated inFig. 4 when biological BDE-209 concentration reaches its maximum
value in September.
As shown in Fig. 11c and d, the mortality ﬂux of phytoplanktonbound BDE-209 in Jiaozhou Bay is higher in August than in February
and decreases from the nearshore area to offshore area. Such a seasonaland spatial variation is similar to the phytoplankton-bound BDE-209
concentration, which is part of the BDE-209 particulate concentration(Fig. 5). The remineralization ﬂux of detritus-bound BDE-209 is also
higher in August than in February and also exhibits an offshore decrease
from estuary areas to the other areas (Fig. 11e & f).
3.3. Budget of BDE-209 in Jiaozhou Bay
To determine the major source and sink of BDE-209 in the bay, weshow the annual ﬂuxes of BDE-209 at four interfaces and those with biogeochemical processes (Fig. 12). The annual ﬂux related to one biogeochemical process is calculated by ∫1365 ∭ F(x, y, z)dxdydzdt, where F (kgm−3 day−1) is a ﬂux due to one biogeochemical process, dx, dy, dz areunit distance (m) in three directions and dt is the unit time interval(day). Before we check the results for each ﬂux, we want to conﬁrm
that the model has reached a steady state. As shown in Fig. 12, over
one year, the standing stock of detritus-bound BDE-209 in the bay
decreases only 0.01 kg, that is 5% of its total amount in the bay. The
dissolved, phytoplankton-bound, and SPM-bound BDE-209 increases

or decreases less than 1% of their total amount in the bay. Therefore,
the model has reached steady state in its second calculation year.
River discharge and air-sea exchange are two sources of BDE-209 in
Jiaozhou Bay. The annually BDE-209 load from rivers to the bay is296.6 kg year−1 and that from air to sea is 3.8 kg year−1. There areseven rivers around the bay, and all have a larger SPM-bound BDE209 load than dissolved BDE-209 load. The total SPM-bound BDE-209
load from rivers is 221.0 kg year−1, and the total dissolved BDE-209
load from rivers is 75.6 kg year−1.
Exchange at the lateral boundary with the Yellow Sea, natural degradation, and sinking to the bottom are the three fates of BDE-209 in Jiaozhou Bay. Annually, the BDE-209 exchange at the lateral boundary with
the Yellow Sea is 273.2 kg year−1, and the decomposition of BDE-209 is
9.1 kg year−1, and the amount of BDE-209 sinking to the bottom is25.1 kg year−1. As an annually averaged value, the mass of dissolved,
phytoplankton-bound, detritus-bound, and SPM-bound BDE-209 is 7.5
kg, 1.1 kg, 0.2 kg, and 34.7 kg, respectively. As shown in Fig. 3, the different forms of BDE-209 would transfer to each other except SPM-boundBDE-209. A total of 38.8 kg year−1 of dissolved BDE-209 is transferredto the phytoplankton-bound form through uptake and absorption, and28.4 kg year−1 of phytoplankton-bound BDE-209 is transferred to thedetritus-bound form through mortality of phytoplankton, and 26.3 kg
year−1 of detritus-bound BDE-209 is transferred to the dissolved form
through the remineralization of detritus.
Based on the mass of BDE-209 and ﬂux of processes removing BDE209 from seawater, the residence time of every form of BDE-209 can becalculated (residence time = mass of BDE-209/ﬂux of processes removing BDE-209 per day). Since there is a report on the residence time ofgroundwater in September in Jiaozhou Bay (Wang et al., 2015a), we
calculated residence time of BDE-209 in September using the monthly
averaged mass and ﬂux of BDE-209. The calculation shows that theresidence time of SPM-bound, dissolved, phytoplankton-bound, andA. Wang et al. / Science of the Total Environment 664 (2019) 522–535

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Fig. 12. Yearly mass balance of BDE-209 (kg year−1) in Jiaozhou Bay calculated by the model. Every arrow represents a biogeochemical process of BDE-209.

detritus-bound BDE-209 in September is 34.0, 30.4, 9.8, and 1.2 day, respectively. The residence time of groundwater is around 30.1–40 day in
September, which is similar to that of SPM-bound and dissolved BDE209 but longer than that of phytoplankton-bound and detritus-boundBDE-209. The reason for such a difference is that SPM-bound and dissolved BDE-209 is removed from seawater mainly through exchange
at the lateral boundary with the Yellow Sea, which is also the process
for groundwater leaving the bay but not mainly for phytoplanktonbound and detritus-bound BDE-209. For SPM-bound BDE-209, 92.2% isremoved through exchange at the lateral boundary with the Yellow
Sea, and 7.8% sinks to the sea bottom. For dissolved BDE-209, 85.7% is removed through exchange at lateral boundary, and 10.2% is decomposed,
and 4.1% is transferred to biological BDE-209. On the other hand, only
25.4% phytoplankton-bound BDE-209 is removed by exchange atlateral boundary and 74.6% is removed by mortality of phytoplankton.
Therefore, phytoplankton-bound BDE-209 has a smaller residence
time than groundwater. The same reason is also true for detritusbound BDE-209 that is removed by remineralization of detritus, sinking,and exchange at the lateral boundary, and their ratios are 94.1%, 2.6%,
and 3.3%, respectively.
4. Discussion

The river-run used the annual mean river discharge, causing the BDE209 from rivers to lose its seasonal variation. The temperature-run
used the annual mean water temperature throughout the calculation.
Similarly, wind-run, chlorophyll-run, and dissolved oxygen-run used
the annual mean wind speed, annual mean chlorophyll concentration,
and annual mean dissolved oxygen concentration, respectively, in thecalculations. Notably, river runoff, water temperature, wind, chlorophyll
a concentration, and dissolved oxygen concentration are changed onlyin the POP module in these experiments.
Compared to other runs, river-run exhibits the largest difference inresults from the control-run for dissolved BDE-209 and SPM-boundBDE-209 (Fig. 13a & b), indicating that the seasonal variation in riversource BDE-209 is the dominant factor controlling the seasonalvariation of dissolved and SPM-bound BDE-209. This is a natural result
if we consider the budget of BDE-209 in the bay (Fig. 12). The differencein biological BDE-209 among all the runs is not as simple as in dissolved
and SPM-bound BDE-209 (Fig. 13c), indicating the impact ofbiogeochemical processes on biological BDE-209 in the bay. The higher
concentration of biological BDE-209 in river-run than in other runs from
December to June (Fig. 13c) is likely caused by the transfer from
dissolved BDE-209 to phytoplankton-bound BDE-209 because there
is a higher dissolved BDE-209 concentration in river-run than in

4.1. Dominant processes responsible for seasonal variation of BDE-209
To investigate the dominant processes responsible for seasonalvariation of BDE-209 concentrations in Jiaozhou Bay, ﬁve sensitivity
calculations were conducted. In each of these calculations, the seasonalvariation in one variable was removed by applying the annual meanvalue of that variable in the model while maintaining the other variables
as those used in calculations shown in Section 3 (hereafter called
control-run). These experiments are named as river-run, temperaturerun, wind-run, chlorophyll-run, and dissolved oxygen-run (Table 2).

Table 2
Conditions of sensitivity experiments.
Name of numerical experimentParameter without seasonal variability

Control-run (Control)
River-run (Ex1-R)
Temperature-run (Ex2-T)
Wind-run (Ex3-W)
Chlorophyll-run (Ex4-Chl)
Dissolved oxygen-run (Ex5-DO)

Rivers discharge of BDE-209
Water temperatureWind speed
Chlorophyll a concentrations
Dissolved oxygen concentrations

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Fig. 13. Time series of dissolved (a) BDE-209, (b) SPM-bound BDE-209, and (c) biological BDE-209 concentrations given by different sensitivity experiments.

other runs in these months (Fig. 13a). Seasonal variation in watertemperature and chlorophyll a concentrations also affects dissolved
and biological BDE-209 because the two types of BDE-209 simulated
by temperature-run and chlorophyll-run are slightly different fromcontrol-run (Fig. 13a, c). From July to October, dissolved BDE-209
concentration is lower in temperature-run than in control-run, whilebiological BDE-209 concentration is higher in temperature-run than incontrol-run. As for chlorophyll-run, the dissolved BDE-209 concentration is a little higher from July to September than in control-run andthe biological BDE-209 concentration is lower; the ﬂuctuation phenomenon of biological BDE-209 from September to November disappears,
indicating that this ﬂuctuation phenomenon is caused by the change
in chlorophyll a concentration. The overlap of results from wind-run
and dissolved oxygen-run with that from control-run in Fig. 13a–cmeans that the seasonal variation in wind speed and in dissolved
oxygen concentration has little inﬂuence on the seasonal variation in
BDE-209 concentration in the bay.
The surface ﬂux is inﬂuenced by the concentration difference between gaseous and dissolved BDE-209, water temperature, and windspeed (Eqs. (A.3)–(A.6)). As shown in Fig. 14a, d, e, f, surface ﬂuxes of
BDE-209 in August and September are from sea to air due to the hightemperature and high dissolved BDE-209 concentration. The time seriesof the calculated surface ﬂux is smoother in wind-run than in other runs

(Fig. 14d), indicating that the high-frequency variation in the surface
ﬂux is caused by high-frequency variation in wind speed. The different
surface ﬂux direction of river-run in summer (Fig. 14b) is caused by alower dissolved BDE-209 concentration; the different surface ﬂux
direction of temperature-run in summer (Fig. 14c) is caused by thelower water temperature. The bottom ﬂux in each run varies little
except for river-run, showing its close dependency on SPM-boundBDE-209 input from rivers (Fig. 13b).
Mechanisms responsible for the seasonal variation in BDE-209 inthese sensitivity runs are given as follows. Compared with controlrun, BDE-209 loads from rivers in river-run is higher in January–Juneand December but lower in July–October, which leads to the similardifference in BDE-209 concentrations between river-run and controlrun (Fig. 13a–c). The difference between net absorption ﬂuxes andremineralization ﬂuxes of detritus-bound BDE-209 can be deﬁned asdar, which affects concentrations of dissolved and biological BDE-209.
When dar is positive, the dissolved BDE-209 concentration decreases
while biological BDE-209 concentration increases; when dar is negative,
the results are inversed. Due to the lower summer water temperature in
the temperature-run, the uptake constant of the phytoplankton matrix(ku) increases and the depuration constant of the phytoplankton matrix(kd) decreases, respectively (Del Vento and Dachs, 2002), which leads
to higher net absorption ﬂuxes of BDE-209 by phytoplankton in

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533

Fig. 14. Time series of daily integrated surface ﬂux and bottom ﬂux of BDE-209 in Jiaozhou Bay calculated by different sensitivity experiments. Black dashed represents the value equal to zero.

temperature-run. Dissolved (biological) BDE-209 concentration in summer is lower (higher) in temperature-run than in control-run becauseof a larger dar in temperature-run than in control-run (Fig. 15a, c). As
shown in Fig. 15a and e, dar is a little greater in control-run than inchlorophyll-run during most of the summer, which causes a slightly
higher dissolved BDE-209 concentration and lower biological BDE-209
concentration in chlorophyll-run than in control-run. On the other
hand, the biological BDE-209 concentration in chlorophyll-run does
not ﬂuctuate from September to November compared with controlrun because of the disappearance of ﬂuctuation in chlorophyll a concentration in chlorophyll-run. The net absorption ﬂux, mortality ﬂux, andremineralization ﬂux in wind-run and dissolved oxygen-run are almost

the same as those in control-run (Fig. 15a, d, f), indicating their negligible role in the biogeochemical processes of BDE-209 in the bay.
Since the understanding on the features of POP sources and behaviors in our study area can be deepened by comparing our work withother similar studies on different POPs in the other regions, we present
a comparison in the Appendix C in Supplementary material.
5. Conclusions
A three-dimensional transport-ecosystem-POP coupled model wasestablished to study the seasonal variation of BDE-209 and related biogeochemical processes in Jiaozhou Bay, a semi-enclosed bay adjacent to

Fig. 15. Time series of daily integrated net absorption ﬂux of dissolved BDE-209, phytoplankton-bound BDE-209 ﬂux through mortality of phytoplankton, and detritus-bound BDE-209 ﬂux
though remineralization of detritus in Jiaozhou Bay, calculated by different sensitivity experiments.

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the Yellow Sea. BDE-209 concentration is higher in summer than inother seasons, and particulate BDE-209 concentration is higher than dissolved BDE-209. Horizontal distributions of dissolved and particulate
BDE-209 concentrations decrease gradually from the nearshore areas
to offshore areas, and the concentrations are vertically homogeneous.
The BDE-209 concentration has a close relation with BDE-209 ﬂuxes
through several interfaces and through biogeochemical processes,
which are affected by runoff of rivers, water temperature and chlorophyll a concentrations. The budget of BDE-209 in the bay indicatesthat the BDE-209 load from rivers is the main source of BDE-209 in
Jiaozhou Bay, and the BDE-209 ﬂux to the Yellow Sea is the main sink.
Sensitivity runs demonstrate that the BDE-209 load from rivers
likely plays the most important role in the seasonal variation ofdissolved and particulate BDE-209 concentrations, and water temperature is the secondary factor. Chlorophyll a also slightly inﬂuences theseasonal variation of BDE-209, while wind speed and dissolved oxygen
have a negligible role in the seasonal variation of dissolved and particulate BDE-209 concentrations.
As a foundational step to a realistic simulation of POP behavior incoastal oceans, the present study demonstrates the seasonal and spatial
variations in BDE-209 concentrations and the mechanisms responsible
for them using a transport-ecosystem-POP coupled model that includes
some primary biogeochemical processes of POPs in the sea. In the POPmodule, however, zooplankton and bacteria are not included, although
they are probably important to the BDE-209 behavior in the ocean.
Furthermore, resuspension of particulate BDE-209 from the sedimentis probably also an important biogeochemical process in shallow waters.
These processes will be included in our model in the near future.
Acknowledgements
This study is funded by the National Nature Science Foundation ofChina (41576010) and the NSFC-Shandong Joint Fund for Marine Ecology
and Environmental Sciences (U1606404). X. Guo thanks support fromthe Fundamental Research Funds for Central Universities of the Ministryof Education of China (201512004). This work is also supported by the
Ministry of Education, Culture, Sports, Science and Technology, Japan(MEXT) to a project on Joint Usage/Research Center–Leading Academia
in Marine and Environment Pollution Research (LaMer). The surface
forcing data of the model is obtained from ECMWF and open boundary
data is obtained from NMEFC.
Appendix. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2019.01.385.
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