Chemosphere 114 (2014) 340–346
Contents lists available at ScienceDirect
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
Occurrence of additive brominated flame retardants in aquatic
organisms from Tai Lake and Yangtze River in Eastern China, 2009–2012
Guanyong Su a, David Saunders b, Yijun Yu a,c, Hongxia Yu a,⇑, Xiaowei Zhang a, Hongling Liu a,
John P. Giesy a,b,d,e
a
State Key Laboratory of Pollution Control and Resource Reuse & School of the Environment, Nanjing University, Nanjing, China
Toxicology Centre, University of Saskatchewan, 44 Campus Drive, Saskatoon, SK S7N 5B3, Canada
Changzhou Environmental Monitoring Center, Changzhou 213001, China
d
Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, SK S7N 5B3, Canada
e
State Key Laboratory in Marine Pollution, Department of Biology and Chemistry, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon,
Hong Kong Special Administrative Region
b
c
h i g h l i g h t s
Temporal trends of PBDEs and HBCDs were investigated in Tai Lake, 2009–2012.
Concentrations of PBDEs showed an upward-trend in the final year.
P
PBDEs with a 100% detection frequency.
P
HBCDs rather than b- or c-HBCD.
HBCDs’ concentrations in samples of Yangtze River were higher than those of Tai Lake.
BDE-47 contributed the greatest proportion of
a-HBCD was the predominate isomer that contributed to
a r t i c l e
i n f o
Article history:
Received 16 October 2013
Received in revised form 6 April 2014
Accepted 18 May 2014
Available online 16 July 2014
Handling Editor: H. Fiedler
Keywords:
PBDEs
HBCDs
Trophic level
Temporal investigation
a b s t r a c t
Since the phase-out of PBDEs, reports regarding occurrences of these compounds in the environment
have become less frequent. To characterize potential influences of the phase-out of PBDEs’ on concentrations in the environment, trends in concentrations as a function of time were investigated for two additive brominated flame retardants, PBDEs and HBCDs. Three aquatic species, including shrimp, common
carp, and yellow catfish, were collected from Meiliang Bay of Tai Lake, 2009–2012. The analysis of PBDEs
in three aquatic organisms has shown a downward-trend in the first three years but a significant upwardtrend in the final year. Concentrations of HBCDs have not shown temporal increases in the investigated
environments. Concentrations of both PBDEs and HBCDs in the three studied organisms increased as a
function of trophic level, which suggested that these additive flame retardants can be biomagnified
through the food web of Tai Lake. In accordance with previous publications, PBDE-47 contributed the
P
greatest proportion of PBDEs and had a detection frequency of 100%. a-HBCD was the predominate isoP
mer that contributed to HBCDs. Both b-HBCD and c-HBCD were likely detected at lesser concentrations
P
than the a-isomer due to differences in bioavailability. Concentrations of PBDEs in the three aquatic
1
organisms from Tai Lake ranged from 1.13 to 97.59 ng g lipid. These concentrations were generally less
than those in biota from other countries, but equal to those found at other locations in China. Specimens
P
from the Yangtze River had greater concentrations of HBCDs (169.6–316.5 ng g1 lipid) than those collected at Tai Lake, which were comparatively greater than many reported concentrations in freshwater
organisms from other countries.
Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction
Due to their low cost and great performance, brominated flame
retardants (BFRs) are widely used in various commercial products,
⇑ Corresponding author. Address: School of the Environment, Nanjing University,
Nanjing 210089, China. Tel.: +86 25 83593649; fax: +86 25 83707304.
E-mail address: yuhx@nju.edu.cn (H. Yu).
http://dx.doi.org/10.1016/j.chemosphere.2014.05.046
0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.
such as furniture, textiles, plastics, paints, and electronic appliances, as a means of reducing their flammability (Lau et al.,
2006; Zhou and Zeng, 2006). Three BFRs, polybrominated diphenyl
ethers (PBDEs), hexabromocyclododecane (HBCDs) and tetrabromobisphenol A (TBBPA), account for the greatest proportion of production of BFRs. TBBPA is a reactive BFR, which is chemically
bound to commercial products and has a limited capacity to leach
G. Su et al. / Chemosphere 114 (2014) 340–346
into the environment. However, HBCDs and PBDEs are generally
used as non-bound additive BFRs, which are simply incorporated
into the product and can gradually leach into the environment during production, usage, and disposal of products. Due to their potential to leach to the environment, additive BFRs have been detected
in various environmental media such as wildlife (Hale et al., 2001;
de Wit, 2002; Pettersson et al., 2004) and humans (Noren and
Meironyte, 2000; Akutsu et al., 2003; Johnson-Restrepo et al.,
2005; Bi et al., 2007). Because of the ubiquity of these compounds
in various environments and potential for toxic effects, PBDEs and
their metabolites had been the subject of numerous studies (Su
et al., 2012a,b).
Many toxicological investigations have shown that PBDEs can
cause various adverse effects to animals, such as nuclear hormone
receptor activity (Meerts et al., 2001; He et al., 2008; Kojima et al.,
2009; Wan et al., 2010), neurotoxicity (Schreiber et al., 2010), or
reproductive effects (Van den Steen et al., 2009). Due to evidence
of toxicity and ubiquity in the environment, in May, 2009, the
Stockholm Convention committees for Persistent Organic Pollutants (POPs) listed the penta-BDE and octa-BDE formulations as
POPs. In October, 2012, the persistent organic pollutants review
committee also adopted a recommendation to include HBCDs in
the Convention’s Annex A for elimination. Though two
technical formulations of PBDEs have been phased-out of production and these chemicals remain at great concentrations in the
environment.
The Yangtze River Delta and Tai Lake, located in East China, are
major production centers for chemicals, textiles, and electronics,
some of which incorporate large amounts of flame retardants such
as PBDEs and HBCDs. The annual production and consumption of
PBDEs in this area have led to PBDE contamination of sediments
(Chen et al., 2006; Shen et al., 2006) and aquatic biota (Xian
et al., 2008). With rapid economic development, new industrial
and commercial enterprises have been established along both sides
of the river into which both polybrominated diphenyl ethers
(PBDEs) and hexabromocyclododecane (HBCDs) have been
reported to be released (Xian et al., 2008; Gao et al., 2009; Xu
et al., 2009). Little information is available regarding temporal
trends of concentrations of PBDEs and HBCDs in this region during
post PBDE phase-out. In this study, three aquatic organisms which
341
represent different trophic levels in Tai Lake, were collected from
2009 to 2012 to characterize the temporal-trends of PBDEs and
HBCDs’ concentrations. Concentration profiles of PBDEs and HBCDs
in Tai Lake and Yangtze River were also compared.
2. Materials and methods
2.1. Sampling
All aquatic samples were collected from Tai Lake (Meiliang Bay)
and from Yangtze River (Nanjing). (Fig. 1) Samples of three species,
including shrimp (Elminius modestus), common carp (Cyprinus carpio) and yellow catfish (Pelteobagrus fulvidraco), were collected
four times during 2009–2012. All samples were selected due to
their occurrence, natural history and feeding guild. These three
species are particularly suitable as sentinel species, as they tend
not to migrate. For comparison, samples of three species of aquatic
organisms, including the common carp, the yellow catfish and the
bigmouth grenadier anchovy (Coilia macrognathos Bleeker), were
collected from the Yangtze River in 2011. Samples were frozen
on site, transported to the laboratory, and were stored at 20 °C
until instrumental analysis. Details regarding the aquatic organisms are provided in Supporting Information (Table S1).
2.2. Chemicals and reagents
The thirteen PBDE congeners (PBDE-17, 28, 71, 47, 66, 100, 99,
85, 154, 153, 138, 183, 190), C13-labeled PBDE-139 and C13-labeled
PCB-178 were purchased from Cambridge Isotope Laboratories
(Andover, MA, USA). The three HBCDs isomers (a-HBCD, b-HBCD,
c-HBCD) and the C13-labeled a-HBCD were purchased from
Wellington Laboratories (Guelph, Ontario, Canada). Solvent
reagents for PBDEs and HBCDs analysis were pesticide residue
grade and purchased from Tedia and Merck.
2.3. Identification and quantification of PBDEs and HBCDs
After measuring the length and weight of individual fish, the
entire fish (at least 3 individuals) was lyophilized and homogenized
Fig. 1. Map of China and the two sampling sites for aquatic organisms: the Yangtze River (Nanjing, Site 1) and Tai Lake (Meiliang Bay, Site 2).
342
G. Su et al. / Chemosphere 114 (2014) 340–346
into one pool and stored frozen until prepared for extraction. Three
replicates from each pool were analyzed.
Concentrations of individual PBDEs were determined by use of
organic solvent extraction, followed by gas chromatography and
mass spectrometry (GC/MS/MS). Approximately 2.0 g of dry fish
sample, to which surrogate standard-13C-PBDE-139 was added,
was extracted by accelerated solvent extraction (ASE, Dionex
ASE-350, Sunnyvale, CA, USA). Extractions were conducted with
n-hexane/dichloromethane (DCM) (1:1) as the first extraction solvent at a temperature of 100 °C and pressure of 1500 psi. Two
10 min. cycles were performed for each solvent. The extract was
concentrated by rotary evaporation to 10 mL, and 2 mL of extract
was taken for gravimetric lipid content determination. The remaining 8 mL of extract was acidified with 10 mL of H2SO4 to remove
lipids. PBDEs were back extracted with a total of 30 mL dichloromethane and hexane (V:V = 1:1) in 3 separate 10 mL extractions.
The organic solvent containing PBDEs was concentrated and
passed through a silica gel column for further clean up. The silica
gel column was packed with glass-wool, activated silica gel
(0.25 g), 44% (w/w) acid silica gel (1.0 g), silica gel (0.25 g), and
anhydrous sodium sulfate (0.30 g) from bottom to top in a disposable Pasteur pipette (Su et al., 2010). The fraction containing PBDEs
and MeO-PBDEs was eluted with 15 mL hexane followed by 15 mL
n-hexane/dichloromethane (1:1). The elution was concentrated by
rotary evaporation and further concentrated to near dryness under
a gentle stream of nitrogen. Then, 9.6 ng of 13C-PCB-178 was added
as the internal injection standard and was re-solubilized with
100 lL hexane prior to GC/MS/MS analysis.
Concentrations of individual HBCDs were determined by use of
organic solvent extraction, followed by gas chromatography and
mass spectrometry (HPLC/MS/MS). Approximately 2.0 g of dry
sample, to which surrogate standard 13C-a-HBCD (Wellington Laboratories, Canada) was added, was Soxhlet extracted with a mixture of acetone and hexane (V:V = 1:1) for 15 h. The extract was
concentrated by rotary evaporation and lipid content was determined gravimetrically. The extract was dissolved in hexane and
acidified with 20 mL H2SO4 to remove lipids. HBCDs was back
extracted with a total of 150 mL hexane in 3 separate 50 mL
extractions. The organic solvent containing HBCDs was concentrated to 1 mL approximately and passed through a silica gel column for further clean up. The silica gel column was packed with
glass-wool, anhydrous sodium sulfate (1 g), silica gel (2 g), 33%
(w/w) acid silica gel (1.0 g), 16.5% silica gel (8 g) and anhydrous
sodium sulfate (1 g) from bottom to top in a disposable Pasteur
pipette. The fraction containing HBCDs was eluted with 100 mL a
mixture of hexane and dichloromethane (1:1). The eluate was concentrated by rotary evaporation and further concentrated to near
dryness under a gentle stream of nitrogen and was re-solubilized
with 100 lL methanol prior to HPLC/MS/MS analysis.
Both the LC and mass spectrometer were controlled by AB Sciex
Analyst 1.4.1 software (Applied Bioscience, Foster City, CA, USA).
An Agilent Eclipse XDB-C18 column was used for chromatographic
separation. Separations were conducted at room temperature. The
volume injected onto the column was 20 lL. Methanol was
selected as the mobile phase at a flow rate of 0.25 mL min1.
HBCDs were detected using a turbo ion spray ion source operated
in the negative ion, multiple-reaction monitoring (MRM) mode.
The ion source and instrumental parameters were optimized prior
to analysis by infusing HBCDs isomers at a concentration of
1 mg L1 into the mass spectrometer. Parameter specific settings
were as follows: DP (30 V), FP (130 V), EP (7 V), Focusing lens
(9) and Prefilter (20). Transitions selected for HBCDs and C13-aHBCD are m/z 640.8–78.9 and 653.0–78.9 (collision energy
50 ev), respectively.
2.5. Quality assurance/quality control
QA/QC was conducted by performing laboratory blanks, GC/MS
detection limit (based on 3S/N) and standard spiked recoveries.
One procedural blank was run with every batch of 6–10 samples
to assess potential sample contamination. Concentrations of target
analytes in laboratory blanks were less than 5% of the sample minimum concentration, which demonstrated that samples were free
from contamination. The limit of detection (LOD) was defined as
the concentration that resulted in a signal-to-noise ratio of 3.
LOD based on 2.0 g of dry sample and instrument sensitivity, varied from congener to congener, from 5.3 to 21.3 pg g1 dry wt. Concentrations less than the LOD were assumed to be non-detects in
calculating summary statistics. Prior to sample analysis, matrix
spikes (n = 4) had been evaluated for each target compound.
Recoveries of matrix spike tests ranged from 71.2% to 128.2% for
each congener of PBDEs and HBCDs. To ensure accuracy of analytical procedures, 13C-labeled PBDE-139 and 13C-labeled a-HBCD
were used as internal standards for PBDEs and HBCDs, respectively.
And the concentration of PBDEs and HBCDs was adjusted according
to the recoveries of the 13C-labeled congeners internal standard.
2.6. Nitrogen isotope measurements
The stable nitrogen isotope ratio in muscle tissue from freshwater fish samples was measured by use of the procedure described
by Sun et al. (1999). Measurements of stable nitrogen isotopes
were used to identify the relative trophic levels of organisms in
the environment. The isotopic ratio was standardized to air according to Eq. (1).
d15 N‰ ¼ fð15 N=14 NÞsample ð15 N=14 NÞair g=ð15 N=14 NÞair 1000
ð1Þ
2.4. Instrumental Analysis
2.7. Statistical analysis
Concentrations of 13 PBDEs were determined by use of a
Thermo Scientific TSQ Quantum GC (USA), coupled with an Agilent
DB-XLB column (15 m 0.25 mm 0.25 lm, USA). The mass spectrometric detector was operated in electron impact ionization (EI)
mode. Samples and standards were analyzed in selected reaction
mode (SRM). Quantification and qualification were processed by
SRM modes. The precursor ion and product ions selected in SRM
mode for each chemical were based on the mass spectrum of the
standard solution. Detailed information about precursor ion, product ions, ions ratios, and collision energy are given in Supporting
Information (Table S2).
Concentrations of HBCDs were determined by use of an Agilent
1200 series HPLC system (Agilent, USA), coupled with an API 3000
triple quadrupole MS/MS system (PE Sciex, Concord, ON, Canada).
Statistical analysis was performed with the OriginPro 8. Spearman rank correlation was used to examine the relationships of
P
P
PBDEs and HBCDs’ concentrations. A Mann–Whitney U nonparametric test was used to compare concentration differences of
target compounds between/among groups (year to year, species
to species). It was considered statistically significant when p < 0.05.
3. Results
3.1. Nitrogen isotope analysis
Organisms at higher trophic levels generally accumulate greater
amounts of 15N. The d15N‰, 3 ± 1‰, was used to discriminate the
different trophic levels. To characterize the relative trophic posi-
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G. Su et al. / Chemosphere 114 (2014) 340–346
tions of organisms, the mean d15N‰ values for shrimp, common
carp, and yellow catfish were determined to be 17.18 ‰, 20.16‰,
and 21.98‰, respectively. Based on the stable nitrogen isotope
ratios in the three aquatic organisms, yellow catfish likely occupied
the highest trophic level followed by the common carp and shrimp.
3.2. Concentrations of PBDEs
In the present study, 10 of 13 targeted PBDEs were detected in
the aquatic organisms from Tai Lake. (Table 1) Three more brominated PBDEs including, PBDE-138, PBDE-183 and PBDE-190, were
not detected in these aquatic organisms. Frequencies of detection
of the 10 detected PBDEs were as follows: PBDE-17 (83%), PBDE28 (92%), PBDE-71 (75%), PBDE-47 (100%), PBDE-66 (8%), PBDE100 (25%), PBDE-99 (25%), PBDE-85 (8%), PBDE-154 (92%) and
PBDE-153 (58%). For all samples from Tai Lake, concentrations of
P
PBDEs ranged from 1.13 to 97.59 ng g1 lipid with mean and
median values of 23.09 ng g1 lipid and 16.48 ng g1 lipid. The
greatest concentration of PBDEs was detected in the yellow catfishes sampled in 2012 (mean: 97.59 ng g1 lipid). Concentrations of
PBDEs in yellow catfish ranged from 29.35 to 97.59 ng g1 lipid
with a mean value of 41.79 ng g1 lipid, which was greater than
that in the common carp (13.93 ng g1 lipid) and shrimp
(11.27 ng g1).
3.3. Concentrations of HBCDs
Only a-HBCD and c-HBCD were detected in aquatic organisms
from Tai Lake and the Yangtze River (Table 2). b-HBCD was not
detected in any sample from both locations. Detection frequencies
for a-HBCD and c-HBCD were 88% and 72%, respectively. ConcenP
trations of
HBCDs ranged from non-detected (ND) to
1
316.5 ng g lipid with mean and median values of 69.36 ng g1
lipid and 28.1 ng g1 lipid in organisms from those two locations.
Inter-species comparison of the three organisms showed concenP
trations of HBCDs in yellow catfish from Tai Lake ranged from
35.2 to 92.1 ng g1 lipid with a mean value of 71.60 ng g1 lipid,
which was significantly greater than concentrations of HBCDs in
shrimp (7.23 ng g1 lipid) or common carp (26.47 ng g1 lipid).
Inter-location comparisons of HBCDs showed that mean concentrations in the yellow catfish and common carp from Yangtze River
were 6.4- and 4.4-fold times greater than concentrations detected
in organisms from Tai Lake, respectively. It is also interesting to
note that migrant fish from the yellow sea returning to the Yangtze
River had significantly lesser HBCDs concentrations than nonmigrant fish.
4. Discussion
In a time-trend study from Sweden from the early 1970s to
1997, concentrations of PBDEs in human milk significantly
increased (Meironyte et al., 1999), while decreases have been
observed for samples since 1996 (Lind et al., 2003). The decrease
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of PBDE concentrations was mainly due to the reduction in concentrations of the PBDE-47 congener. Similar decreasing temporal
trends in blood of newborns has been observed from 1997 to 2011
in New York state (Ma et al., 2013). In May, 2009, the commercial
penta-BDE and octa-BDE formulations were listed as POPs and
banned worldwide. The ban of two technical formulations of PBDEs
might have a strong impact on the environmental concentrations
of PBDEs and their potential substitute compounds (Covaci et al.,
2006), such as HBCDs. Here, the analysis of PBDEs in three aquatic
organisms collected from Tai Lake and the Yangtze River from 2009
to 2012, has shown a downward-trend in the first three years but a
significant upward-trend in the final year (Fig. 2). Specifically, concentrations of PBDEs in aquatic organisms have been compared
with those reported in previous publications at Tai Lake and the
Yangtze River sampling sites (Gao et al., 2009). Due to the disposal
of waste containing PBDEs and the persistence of these compounds, it can be inferred that they would continue to exist at high
concentrations in the environment surrounding Tai Lake and the
Yangtze River. Only slight temporal variations in concentrations
of HBCDs have be observed from 2009 to 2012, which indicates
that concentrations of HBCDs in the environment have not been
influenced by the phase-out of PBDEs (Fig. 3).
Table 1
Concentrations of PBDEs in aquatic organisms from the Tai Lake, China.
a
Locations Common
name
Latin
name
Taihu
Shrimp
(2009)
Common
carp
Yellow
catfish
E. modestus
Fat
content
(%)
5.7
Cyprinus carpio
15.3
Pelteobagrus
fulvidraco
21.3
Taihu
Shrimp
(2010)
Common
carp
Yellow
catfish
E. modestus
15.0
Pelteobagrus
fulvidraco
17.3
Taihu
Shrimp
(2011)
Common
carp
Yellow
catfish
E. modestus
7.0
Taihu
Shrimp
(2012)
Yellow
catfish
E. modestus
Cyprinus carpio
6.6
Cyprinus carpio
16.9
Pelteobagrus
fulvidraco
14.0
Pelteobagrus
fulvidraco
‘‘ND’’ means not detected.
9.1
10.8
Concentration (unit: ng g1 lipid)
PBDE-17 PBDE-28
PBDE-71 PBDE-47
PBDE66
PBDE100
PBDE99
PBDE85
PBDE154
PBDE153
nd
0.13–
0.15
nd
0.11–
0.13
nd
0.01–
0.05
nd
0.28–
0.30
0.37–
0.43
nd
0.20–
0.24
0.59–
0.85
0.60–
0.62
0.21–
0.29
0.22–
0.24
nd
P
PBDEs
1.04–
1.00–1.22 nda
1.08
1.81–2.6 1.11–1.43 3.62–
5.17
3.20–
1.51–1.71 4.32–
3.62
4.50
11.00–
16.66
9.87–
12.05
18.37–
18.77
0.23–
0.65
2.36–
2.65
7.32–
10.80
0.07–0.20 nd
0.47–0.64 nd
nd
nd
nd
nd
nd
1.13
2.98–4.97 0.86–
2.11
0.68–1.70 3.56–
4.08
6.46–9.42 nd
nd
nd
nd
nd
16.48
9.03–
10.83
nd
nd
nd
0.52–
0.63
3.39–
3.76
0.59–
1.04
28.80
0.10–
0.25
1.30–
1.48
2.66–
2.84
0.10–0.30 0.18–
0.18
0.20–0.61 1.06–
2.22
0.54–0.73 1.61–
2.08
1.12–1.40 nd
nd
nd
nd
nd
3.14
0.62–2.18 nd
nd
nd
nd
nd
5.54
3.61–4.18 nd
nd
nd
nd
0.06–
2.59
0.54–
0.86
1.91–
2.02
0.15–
0.46
11.40
4.06–
4.50
nd
1.10–1.62 nd
16.08–
20.72
44.28–
56.55
nd
nd
nd
nd
0.75–
1.55
0.39–
0.77
nd
0.10–
0.26
6.00–
16.53
24.56
nd
0.21–
0.46
3.82–
17.57
11.36–
14.59
8.72–
12.29
nd
nd
0.36–
0.45
16.26
19.78
29.35
97.59
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G. Su et al. / Chemosphere 114 (2014) 340–346
Table 2
Concentrations of HBCDs in aquatic organisms from the Tai Lake and Yangtze River, China.
Locations
a
Common name
Latin name
Fat content (%)
Concentration (unit: ng g1 lipid)
a-HBCD
b-HBCD
c-HBCD
P
HBCDs
Taihu (2009)
Shrimp
Common carp
Yellow catfish
E. modestus
Cyprinus carpio
Pelteobagrus fulvidraco
5.7
15.3
21.3
nda
45.0–51.6
29.2–33.2
nd
nd
nd
nd
3.1–3.11
3.4–4.6
nd
51.9
35.2
Taihu (2010)
Shrimp
Common carp
Yellow catfish
E. modestus
Cyprinus carpio
Pelteobagrus fulvidraco
15.0
6.6
17.3
nd–4.5
nd
80.9–99.1
nd
nd
nd
nd
nd
2.1–2.1
2.3
nd
92.1
Taihu (2011)
Shrimp
Common carp
Yellow catfish
E. modestus
Cyprinus carpio
Pelteobagrus fulvidraco
7.0
16.9
14.0
7.3–17.1
14.9–28.0
71.9–77.3
nd
nd
nd
nd–3.9
1.4–3.0
3.1–4.5
14.2
23.7
78.4
Taihu (2012)
Shrimp
Yellow catfish
E. modestus
Pelteobagrus fulvidraco
9.1
10.8
3.5–5.7
72.7–87.9
nd
nd
nd–1.1
nd–0.8
5.2
80.7
Yangtze River (2011)
Common carp
Yellow catfish
Bigmouth grenadier anchovy
Cyprinus carpio
Pelteobagrus fulvidraco
Coilia macrognathos Bleeker
9.6
20.8
37.5
160.0–174.4
254.2–356.7
25.6–26.5
nd
nd
nd
4.0–4.8
8.2–13.8
1.4–2.6
169.6
316.5
28.1
‘‘ND’’ means not detected.
P
Fig. 2. Concentration distributions of PBDEs in aquatic organisms from Tai Lake,
Eastern China (‘‘TL’’ means ‘‘Tai Lake’’; ‘‘YR’’ means ‘‘Yangtze River’’.).
P
Fig. 3. Concentration distributions of HBCDs in aquatic organisms from Tai Lake
and Yangtze River, Eastern China (‘‘TL’’ means ‘‘Tai Lake’’; ‘‘YR’’ means ‘‘Yangtze
River’’.).
Biomagnification of PBDEs and HBCDs has been reported at significant levels through various freshwater food webs (Wu et al.,
2009), which indicates that concentrations of these chemicals will
increase with increasing trophic level. A similar trend was
observed here. Based on the d15N‰ content analysis in this investigation, the three aquatic organisms occupy different trophic
levels in their respective food webs. Evidence of bioaccumulation
of PBDEs and HBCDs in a freshwater food web in Tai Lake have
been observed: shrimp (PBDEs: 11.27 ng g1; HBCDs: 5.43 ng g1;
d15N‰: 17.18‰) < common carp (PBDEs: 13.93 ng g1; HBCDs:
19.85 ng g1; d15N‰: 20.162‰) < and the yellow catfish (PBDEs:
41.79 ng g1; HBCDs: 71.6 ng g1; d15N‰: 21.975‰).
P
Concentrations of
PBDEs in aquatic organisms from the Tai
Lake were generally less than those in biota from other countries
(Darnerud, 2003; Kiviranta et al., 2004; Schecter et al., 2004,
2006), but equal to those concentrations found in other locations
in China (Meng et al., 2007; Gao et al., 2009). Fish from Tai Lake
had concentrations of PBDEs which ranged from 0.87 to
195.17 ng g1 lipid, which were lesser than concentrations in fish
from the USA (1100 pg PBDE g1 ww) (Schecter et al., 2004,
P
2006), Spain (330 pg PBDE g1 ww) (Bocio et al., 2003), Sweden
P
1
(630 pg PBDE g ww) (Darnerud et al., 2006), Finland (850 pg
P
PBDE g1 ww) (Kiviranta et al., 2004) and Japan (910 pg
P
P
PBDE g1) (Ohta et al., 2002). Mean concentrations of PBDEs
in fish were similar to those detected in fish from Guangdong,
P
South China (160 pg
PBDE g1 ww) (Meng et al., 2007; Gao
et al., 2009). Similarly, concentrations of PBDEs in shrimp from
Tai Lake were lesser than those from other countries, such as the
Netherlands (1765–2962 ng g1 lipid) (Verslycke et al., 2005), Belgium (ND-8.3 ng g1 ww) (Voorspoels et al., 2003) and Canada
(48 pg g1 ww) (Tittlemier et al., 2004). Concentrations of PBDEs
in shrimp were similar to those from other locations in China
P
(Gao et al., 2009). Concentrations of HBCDs in fish from the Yangtze River ranged from 169.6 to 316.5 ng g1 lipid, which were significantly greater than those (ND-92.1 ng g1 lipid) from Tai Lake.
Previous investigations have also shown that concentrations of
P
HBCDs in the Yangtze River were similar or greater than those
from other countries, but were generally lower than concentrations detected at contaminated sites or downstream of point
sources (Covaci et al., 2006). The high concentrations of HBCDs
detected in the Yangtze River are in accordance with several previous publications (Xian et al., 2008; Li et al., 2013), however, the
ultimate source of HBCDs is still unknown. In this investigation,
concentrations of PBDEs and HBCDs were positively correlated,
indicating a similar property between these two chemicals (Pearson corrections; r2 = 0.57; p = 0.05).
Similar to previous publications, PBDE-47 contributed the
P
greatest proportion to PBDEs and had a detection frequency up
G. Su et al. / Chemosphere 114 (2014) 340–346
to 100%. In this analysis, PBDE-17, PBDE-28, PBDE-71 and PBDEP
154 were also predominant congeners contributing to
PBDEs,
which is consistent with results of previous investigations. PBDE138, PBDE-183 and PBDE-190, were not detected in any aquatic
organism, which might indicate that PBDEs congeners with greater
degrees of bromination were not readily accumulated by aquatic
organisms. The deficit of heavier PBDE congeners in this analysis
might be related to the source profile or their limited aqueous solubilities. In this research, the a-HBCD isomer was detected at the
greatest concentrations and frequencies in aquatic organisms,
which corresponds with previous publications (Isobe et al., 2007;
Xian et al., 2008). However, the stereochemical analysis of commercial HBCDs mixtures has shown that the content of a-HBCD,
b-HBCD and c-HBCD was 10–13%, 1–12% and 75–89%, respectively
(Heeb et al., 2005). Though the c-HBCD isomer comprises the
greatest proportion of the HBCDs commercial mixture, the isomer
is known to undergo rapid hepatic biotransformations to other diastereomers and metabolites, and fecal/urinary elimination (Hakk
et al., 2012). In contrast, the a-HBCD isomer is more biologically
persistent, resistant to metabolism, has a longer biological half-life
of up to 21 d and bioaccumulates in lipid-rich tissues (Szabo et al.,
2011).
5. Conclusions
Since the phase-out of PBDEs in 2009, two additive brominated
flame retardants (PBDEs and HBCDs) were determined in three
aquatic species (shrimp, common carp, and yellow catfish). Concentrations of PBDEs were decreasing during the first three years,
but then increased during the last year. This investigation has
shown that both PBDEs and HBCDs were bioaccumulated in a
freshwater food web in Tai Lake. Aquatic species from Yangtze
River were contaminated by HBCDs more heavily than those from
Tai Lake. Despite the phase-out of penta-BDEs, PBDE-47 still conP
tributed the greatest proportion to PBDEs. Comparisons between
HBCDs isomers showed that a-HBCD was detected at the greatest
concentrations and frequencies in aquatic organisms, likely due to
their specific biological properties.
Acknowledgement
This work was supported by the National Natural Science
Foundation of China (No. 21377053). Prof. Giesy was supported
by the program of 2012 ‘‘High Level Foreign Experts’’
(#GDW20123200120) funded by the State Administration of
Foreign Experts Affairs, the P.R. China to Nanjing University and
the Einstein Professor Program of the Chinese Academy of Sciences.
He was also supported by the Canada Research Chair program, a
Visiting Distinguished Professorship in the Department of Biology
and Chemistry and State Key Laboratory in Marine Pollution, City
University of Hong Kong.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.chemosphere.
2014.05.046.
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1
Occurrence of additive brominated flame retardants (PBDEs and HBCDs) in aquatic
2
organisms from Tai Lake and Yangtze River in Eastern China, 2009-2012
3
Guanyong Su1; David Saunders2; Yijun Yu1,3; Hongxia Yu1*; Xiaowei Zhang1; Hongling Liu1; John P.
Giesy1,2,45
4
5
6
7
8
1
9
2
Toxicology Centre, University of Saskatchewan, 44 Campus Drive, Saskatoon, SK, Canada, S7N 5B3
10
3
Changzhou Environmental Monitoring Center, Changzhou, 213001, China
11
12
4
13
14
5
State Key Laboratory of Pollution Control and Resource Reuse & School of the Environment, Nanjing
University, Nanjing, China
Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, SK, Canada S7N
5B3
State Key Laboratory in Marine Pollution, Department of Biology and Chemistry, City University of Hong
Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong SAR, China
15
16
17
18
19
20
21
22
23
24
25
26
Authors for correspondence:
School of the Environment
Nanjing University
Nanjing, 210089, China
Tel: 86-25-83593649
Fax: 86-25-83707304
E-mail:
yuhx@nju.edu.cn (Hongxia Yu)
27
Supporting Table 1 Details of the collected aquatic samples in Tai Lake and Yangtze Rivera
Locations
Sampling
time
2009.07
2010.07
Tai Lake
2011.07
2012.07
Yangtze River
(2011)
28
29
30
Common name
Latin name
Number
Length
Wet weight
the shrimpb
E. modestus
the common carp
Cyprinus carpio
3
12-16 cm
68.2-102.9 g
the yellow catfish
Pelteobagrus fulvidraco
3
13-19 cm
81.9-115.4 g
the shrimp
E. modestus
the common carp
Cyprinus carpio
3
15-17 cm
147.2-168.9 g
the yellow catfish
Pelteobagrus fulvidraco
3
11-22 cm
35.6-121.3 g
the shrimp
E. modestus
the common carp
Cyprinus carpio
3
14-17
89.3-114.5 g
the yellow catfish
Pelteobagrus fulvidraco
3
14-18
23.3-84.1 g
the shrimp
E. modestus
the yellow catfish
Pelteobagrus fulvidraco
9
7-22 cm
22.2-131.4 g
the common carp
Cyprinus carpio
3
26-33 cm
420.7-885.3 g
the yellow catfish
Pelteobagrus fulvidraco
32
10.0-14.0
11.7-32.6
the bigmouth grenadier
Coilia macrognathos
anchovy
Bleeker
9
20.0-26.0
30.0-65.8 g
116.7 g
247.5 g
430.6 g
543.8
2011.07
a. For each species, at least 3 individuals were pooled together and run for the instrumental analysis in three replicates.
b. Due to the shrimps’ small size, the number of shrimp was not counted by us.
31
Supporting Table 2 Ion pairs, abundance ratio and collision energy of selected reaction mode.
Ion pairs for Quantification and Qualification
Chemicals
32
Collision Energy (eV)
Parent Ion
Product Ion
Abundance Ratio
PBDE-17
245.88
245.88, 138.85
100/30
20
PBDE-28
245.88
245.88, 138.86
100/12
20
PBDE-71
325.66
216.79, 218.94
92/100
30
PBDE-47
325.66
216.79, 218.95
61/100
30
PBDE-66
325.66
216.79, 218.96
100/93
30
PBDE-100
405.63
296.60, 405.63
100/44
30
PBDE-99
405.63
296.60, 405.64
100/40
30
PBDE-85
405.63
296.60, 405.65
100/28
30
PBDE-154
483.64
483.64, 402.57
42/100
30
PBDE-153
483.64
483.64, 402.58
18/100
30
PBDE-138
483.64
483.64, 402.59
5/100
30
PBDE-183
563.73
563.73, 485.15
5/100
30
PBDE-190
563.73
563.73, 485.15
5/100
30