Environment International 127 (2019) 226–232

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Environment International
journal homepage: www.elsevier.com/locate/envint

Biomagnification of PBDEs and alternative brominated flame retardants in a T

predatory fish: Using fatty acid signature as a primer
⁎
Lin Taoa,b, Ying Zhangc, Jiang-Ping Wud, , Si-Kang Wud, Yu Liua,b, Yan-Hong Zenga,
⁎
Xiao-Jun Luoa, Bi-Xian Maia,
a
State Key Laboratory of Organic Geochemistry and Guangdong Key Laboratory of Environmental Resources Utilization and Protection, Guangzhou Institute of
Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China
b
University of Chinese Academy of Sciences, Beijing 100049, China
c
Scientific Institute of Pearl River Water Resources Protection, Monitoring Center of Pearl River Valley Aquatic Environment, Guangzhou 510611, China
d
College of Environmental Science and Engineering, Anhui Normal University, Wuhu 241002, China

A R T I C LE I N FO A B S T R A C T

Handling Editor: Heather Stapleton Information on biomagnification of alternative brominated flame retardants (ABFRs) is limited and results are
Keywords: inconclusive, due in part to uncertainty in the understanding of predator/prey relationships. In the present
Alternative BFRs study, a predatory fish, Channa argus, and several forage fish species were obtained from an ABFR contaminated
PBDEs site. The predator/prey relationships were identified based on fatty acid (FA) signatures in the predator and
Biomagnification prey. Biomagnification factors (BMFs) for several ABFRs including decabromodiphenyl ethane (DBDPE), 1,2‑bis
Diet composition (2,4,6‑tribromophenoxy) ethane (BTBPE), hexabromobenzene (HBB), pentabromotoluene (PBT), and pentab-
Fatty acid signature romoethylbenzene (PBEB) were estimated based on the identified predator/prey relationships. The results
showed that crucian carp was the main prey of C. argus, contributing to 71%–100% to its total diet. The mean
BMFs for DBDPE, BTBPE, and HBB were 0.06, 0.40, and 0.91, respectively, indicating trophic dilution of these
ABFRs. However, biomagnification of PBT and PBEB, with BMFs of 2.09 and 2.13, respectively, was observed.
The BMFs for PBT, PBEB and HBB were comparable to or even higher than those for some polybrominated
diphenyl ether (PBDE) congeners estimated in the same individual predator, indicating that these emerging
pollutants may pose significant environmental risks. The BMFs for ABFRs and PBDEs were significantly and
negatively correlated to the log KOWs of these chemicals, suggesting that the biomagnification of these chemicals
was depressed due to their superhydrophobic nature.

1. Introduction persistent organic pollutants (POPs) by the Stockholm Convention and

Brominated flame retardants (BFRs) are synthetic chemicals that
have been extensively used in products to impede ignition (de Wit,
2002). Three major BFRs, polybrominated diphenyl ethers (PBDEs),
hexabromocyclododecanes (HBCDs) and tetrabromobisphenol‑A
(TBBP-A), have been widely added to consumer products such as
plastics, textiles, furniture, and electric/electronic devices. Most of
these chemicals are simply blended with the polymers and are not
chemically bound to the products. Thus, they can be released into the
environment during the production, use, and disposal of the BFR-con-
taining products (de Wit, 2002). Once in the environment, these BFRs
are persistent, bioaccumulative and toxic to wildlife and humans (Wu
et al., 2011; Yu et al., 2016). Due to their high ecological and health
risks, commercial PBDE and HBCD formulations are currently listed as
have been heavily restricted globally (Stockholm Convention, 2017).
To maintain fire safety levels, some non-regulated flame retardants,
e.g., decabromodiphenyl ethane (DBDPE), 1,2‑bis(2,4,6‑tri-
bromophenoxy) ethane (BTBPE), hexabromobenzene (HBB), pentab-
romotoluene (PBT), and pentabromoethylbenzene (PBEB), have been
used as alternatives for the discontinued BFRs (Covaci et al., 2011).
DBDPE and BTBPE have been used for > 20 years as replacements of
commercial Deca- and Octa-BDE formulations, respectively (Munschy
et al., 2015). HBB, PBT, and PBEB were used as additive flame re-
tardants in paper, woods, textiles, electronic and plastic goods, and
thermoset polyester resins, and are still produced in Asia currently
(Covaci et al., 2011; Munschy et al., 2015). Similar to the discontinued
BFRs, these alternative brominated flame retardants (ABFRs) can be
released into the environment and some of them have become

⁎
Corresponding authors.
E-mail addresses: jpwu@ahnu.edu.cn (J.-P. Wu), nancymai@gig.ac.cn (B.-X. Mai).

https://doi.org/10.1016/j.envint.2019.03.036
Received 1 December 2018; Received in revised form 13 March 2019; Accepted 14 March 2019
Available online 28 March 2019
0160-4120/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
L. Tao, et al.
ubiquitous (Wolschke et al., 2015; Vorkamp et al., 2015). After the
phase out of PBDEs and HBCDs, there was a shift from legacy BFRs to
ABFRs in the environment (Zhu et al., 2014; Yadav et al., 2017;
Wolschke et al., 2015). Because of their highly lipophilic properties, the
ABFRs can be potentially accumulated in biota and biomagnified in
food chains (Wu et al., 2010, 2011; Sun et al., 2015).
Biomagnification potential is one of the vital criterions for assessing
the ecological risks of a chemical, especially those of emerging pollu-
tants (Cristale et al., 2013). Only a few investigations have been per-
formed on the biomagnification potentials of ABFRs. Furthermore, the
results on biomagnification potential of ABFRs are inconclusive. DBDPE
was found to be biomagnified in some predatory fishes from a Lake
Winnipeg (Canada) and in a mangrove food web in South China (Law
et al., 2006; Sun et al., 2015), but was found to be biodiluted as ob-
served in some predator/prey relationships from Lake Winnipeg and in
a fish-eating bird, common kingfisher, from an e-waste recycling site in
South China (Law et al., 2006; Mo et al., 2012). Similarly, BTBPE
showed relatively high biomagnification potential in some predator/
prey pairs like walleye/white fish and emerald shiner/zooplankton
from Lake Winnipeg and in common kingfisher from an e-waste re-
cycling site, with biomagnification factors (BMFs) > 1 (Law et al.,
2006; Mo et al., 2012). However, BMFs for BTBPE were lower than 1 in
some predator/prey relationships such as walleye/emerald shiner and
white suckers/mussels from Lake Winnipeg (Law et al., 2006). The
observed discrepancies in the biomagnification potentials of ABFRs
could be due to the uncertainties in the predator/prey relationships,
trophic level differences between predators and preys across studies,
and/or lower potential for biomagnification of the ABFRs. The com-
plexity of results obtained in earlier studies warrant further research
using suitable methods to estimate the diet composition and the con-
tribution of each food components of a predator, to better understand
the biomagnification potentials of ABFRs and assess their ecological
risks.
Determination of fatty acid (FA) signatures is an effective method to
investigate the diet composition of a predator and assess the sources of
pollutants in the predator (Satterthwaite-Phillips et al., 2014; Magnone
et al., 2015; McKinney et al., 2009, 2010). FAs are the major con-
stituents of most lipids. Unlike other nutrients that are readily degraded
(e.g., proteins), specific FAs remain intact during digestion and can be
conservatively transferred to higher trophic levels (Iverson et al., 2004;
Budge et al., 2012), potentially reflecting the diets of many organisms
over a long time span. Moreover, several FAs cannot be biosynthesized
by animals (Cook, 1991), which makes it possible to distinguish be-
tween dietary components and nondietary components. Controlled
feeding experiments demonstrated that diet compositions of a predator
inferred through FA signatures are highly accurate (Nordstrom et al.,
2008; Happel et al., 2016). Quantitative fatty acid signature analysis
has also been successfully used to analyze the diet compositions of
several predators in the field, including marine mammals (Thiemann
et al., 2008; Meynier et al., 2010; Bromaghin et al., 2013), seabirds
(Wang et al., 2010), and fish (Magnone et al., 2015; Happel et al.,
2016). Differences in FA signatures between a predator and its forage
species were also used to assess the sources of POPs in a predator
(Wolkers et al., 2006; McKinney et al., 2009, 2010). By comparing the
FA profiles between the predator and its prey, Wolkers et al. (2006)
indicated that the differences in contaminant levels and profiles found
in walruses from eastern Svalbard were possibly due to variations in
their feeding habits. Also based on FA analysis and supplemented by
stable nitrogen and/or carbon isotope technique, McKinney et al.
(2009, 2010) revealed that the differences in the levels of poly-
chlorinated biphenyls (PCBs), PBDEs, and dichlorodiphenyltri-
chloroethane (DDT) found in killer whales from diverse habitats were
related to their correspondingly variable diets. It was suggested that the
stable isotope-approach is often underdetermined, and consumer stable
isotope fractionation is often unknown (Brett et al., 2016). The use of
FA signatures provides an alternative approach that can resolve the
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Environment International 127 (2019) 226–232
underdetermined constraint (Brett et al., 2016).
The aim of the present study was to assess the biomagnification
potential of ABFRs in a contaminated predatory fish, northern snake-
head (Channa argus), using FA signatures as indicators of the dietary
composition of this predator. We measured the levels of several ABFRs,
including DBDPE, BTBPE, HBB, PBT and PBEB, and PBDEs in C. argus
and its potential forage species. FA profiles in the predator and the prey
species were also examined to provide quantitative estimates of the
contribution of each prey species to the total diet of the predator. BMFs
of ABFRs were calculated based on dietary composition, and compared
with those of PBDEs to assess the biomagnification potential of these
emerging pollutants.
2. Materials and methods
2.1. Sampling
Sampling was conducted at an e-waste recycling site located in
Qingyuan City, Guangdong Province, China (23°36′N, 113°04′E) in
2016. PBDEs and ABFRs are common pollutants at e-waste recycling
sites, due to the rudimentary e-waste recycling processes, including
open burning and acid washing (Wu et al., 2008). Northern snakehead
(C. argus; n = 15) was collected from a natural pond at the e-waste
recycling site. According to the available information regarding the
prey of northern snakehead (Tian, 1997), a comprehensive sampling of
the possible forage species was carried out in the pond during the same
time span. The potential prey species included mud carp (Cirrhinus
molitorella; n = 18), Chinese bitterling (Rhodeinae, n = 6), crucian carp
(Carassius auratus, n = 7), tilapia (Oreochromis spp, n = 9), shrimp
(Neocaridina denticulata, n = 108), dragonfly larvae (Aeshnidae rambur,
n = 18), and water beetles (Sternolophus inconspicuus, n = 16). Some
species (shrimp, dragonfly larvae and water beetles) were too small to
analyze contaminants in individuals and were therefore pooled. After
being transported to the laboratory, all the samples were stored at
−20 °C until further analysis.
2.2. Contaminant extraction, clean-up, and analysis
The extraction, clean-up, and chemical analyses were performed
using established methodologies for analysis of BFRs in biota samples
(Peng et al., 2015), with minor modifications. In brief, all samples were
freeze-dried. After spiked with BDEs 77, 181, 205 and 13C-BDE 209 as
surrogates, the samples were Soxhlet extracted using an acetone/
hexane mixture. The extract was purified using concentrated sulfuric
acid and further cleaned by passing through a multi-layer silica column
packed with neutral silica, acid silica and anhydrous sodium sulfate.
The levels of ABFRs and PBDEs were determined using a gas chroma-
tograph (GC) coupled with a mass spectrometer (MS). For more details
on the extraction, clean-up, and analysis of the contaminants and
quality control measures, please refer to Peng et al. (2015) and the
Supplementary Data section.
2.3. FA extraction, methyl esterification, and analysis
Lipids were extracted from the dorsal muscle of C. argus and from
whole body of the prey species according to Bligh and Dyer (1959),
with minor modifications. Briefly, after the spiking of FA 21:0 as a
surrogate standard, approximately 0.1–0.2 g of the sample was ex-
tracted with a dichloromethane/methanol mixture (2:1, v/v) con-
taining 0.01% butylated hydroxytoluene (BHT), using an ultra-
sonicator. An aliquot of the extract was used for lipid content
determination using a gravimetric method. The remainder of the ex-
tract was transesterified to FA methyl esters (FAME) by adding an
acidic methanol solution. The solution was then centrifuged and the
resulting upper layer containing FAME was collected. The concentra-
tions of the FAMEs were analyzed using a GC equipped with a flame
L. Tao, et al.
ionization detector (FID). A detailed description of the method is given
in the Supporting Information.
2.4. Estimation of the dietary composition of northern snakehead
The dietary composition of northern snakehead based on FA sig-
natures was estimated according to a previously reported method
(Iverson et al., 2004). In brief, a set of 16 FAs that typically made
up > 0.2% of ∑FAs was selected from the 37 individual FAs measured
in the present study. We only selected FAs with concentrations > 0.2%
considering that the quantification of FA is not accurate when its con-
centration is too low (< 0.2%) based on the limits of quantification of
the FA determination method used in our study. All FAs were normal-
ized to 100% before the estimation of diet composition. We used a
distance minimizing method to infer the diet, by determining the prey
FA signature combinations that were closest to the real FA profiles of
the predator. The estimated proportion of certain FA in the predator, as
a weighted combination of that FA in the prey, was calculated using Eq.
(1):
ŷ= ∑ p k xk
k (1)
where ŷ is the estimated proportion of the FA in the predator, xk is the
mean proportion of FA in the prey type k, and pk refers to the estimated
proportion of the prey type k in the predator's diet.
Our purpose was to estimate pk so that the estimated ŷ is as similar
to the real y as possible. According to Iverson et al. (2004), we used the
Kullback-Liebler (KL) distance to compare the FA profiles. The KL is
calculated according to Eq. (2):
yj
KL = ∑ (yj − ŷj) log ⎛⎜ ŷ ⎞⎟
j ⎝ j⎠ (2)
where ŷj is the estimated proportion of the j FA of the predator, yj is
th
the real proportion of the jth FA of the predator.
We carried out an optimization using MATLAB to determine pk
when KL had a minimum value. The optimization was initialized with
an equal value for pk. It was assumed that all the prey contained the
same lipid content when estimating pk values, therefore, the calculated
pk values were then adjusted by the average lipid content of each prey
type. Details on the methods used to estimate the dietary composition
of northern snakehead are described in the Supplementary Data section.
2.5. BMF estimation
Biomagnification factor (BMFFA) of the target compounds was es-
timated based on the diet composition of the predator. The BMFFA was
calculated using Eq. (3):
BMFFA = Cpredator / ∑ pk Ck
(3)
k
where Cpredator is the concentration (ng/g lipid weight) of the target
compound in the predator (northern snakehead), Ck is the mean con-
centration (ng/g lw) of compound in prey type k, and pk refers to the
estimated contribution of the prey type k to the predator's total diet.
3. Results and discussion
3.1. Levels and profiles of ABFRs
Concentrations of ABFRs in northern snakehead and its potential
forage species are presented in Table 1. Species-specific accumulation
of ABFRs was observed in the current samples. Tilapia
(13,500 ± 4220 ng/g lw) and dragonfly larvae (28,000 ± 4850 ng/g
lw) harbored the highest ∑ABFRs concentrations, being 1–2 orders of
magnitude greater than the other species examined (Table 1). In
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Environment International 127 (2019) 226–232
contrast, the lowest ∑ABFRs concentration was observed in Chinese
bitterling (128 ± 28.0 ng/g lw). The variation in ∑ABFRs concentra-
tions among species might be attributable in part to species-specific
ecological status such as feeding habits and trophic level. Tilapia feeds
on organic detritus or decomposed organic matter which contains high
concentrations of hydrophobic organic chemicals, rendering them
prone to higher exposure to ABFRs compared to the other species.
Dragonfly larvae are carnivorous insects and exist at a relatively high
trophic level, resulting in high ABFRs in their body due to biomagni-
fication of these chemicals. In contrast, Chinese bitterling is phyto-
phagous. It is not surprising that Chinese bitterling contained relatively
low ∑ABFRs concentrations because of their relatively low trophic level.
E-waste recycling site has been demonstrated to be a hotspot of
ABFRs (Wu et al., 2012). Concentrations of ABFRs have been previously
reported in fish and prawn from the e-waste recycling site considered in
the current study site (Wu et al., 2010; Liu et al., 2018a). The levels of
DBDPE in mud carp and shrimp determined in the present study were of
the same order of magnitude as those in common carp
(median = 620 ng/g lw) and prawn (340 ng/g lw) recently sampled
from this e-waste recycling site (Liu et al., 2018a). However, the levels
of DBDPE recorded in northern snakehead and crucian carp were > 2
orders of magnitude higher than those (up to 14.0 ng/g lw) in these
species collected in 2006 (Wu et al., 2010). This could be due to the
changes in the usage of flame retardant added to electrical and elec-
tronic equipment, with a predominant use of DBDPE after the ban of c-
Deca-BDEs (Munschy et al., 2015). BTBPE concentrations in mud carp
and crucian carp were of the same order of magnitude as those (med-
ians of 518 ng/g lw in mud carp and 323 ng/g lw in crucian carp)
previously reported in the same species (Wu et al., 2010); but in
northern snakehead, the current level was 2 orders of magnitude higher
than that (1.71 ng/g lw) previously reported in this species (Wu et al.,
2010). The concentrations of HBB, PBT and PBEB, in fish and shrimp
samples in the present study were of the same magnitude as reported in
fish and prawn species collected from the same e-waste recycling site
(Wu et al., 2010; Liu et al., 2018a).
To compare the levels of ABFRs and PBDEs, the concentration ratios
of ∑ABFRs to ∑PBDEs in the current fish, shrimp and insects were fur-
ther calculated (Fig. 1). The mean ratios ranged from 0.08 in northern
snakehead to 0.38 in water beetles, indicating the lower fractions of
ABFRs compared with PBDEs. This is contradicted by the findings re-
cently reported in environmental samples collected from South China,
which showed that ABFRs are the predominant BFRs (Zhu et al., 2018).
The discrepancy may likely mirror the BFR use history, that is, the e-
waste being processed is “older” electrical and electronic equipment
which was produced when PBDE use was not restricted.
As illustrated in Fig. 2, the profiles of the investigated ABFRs varied
among species. DBDPE was the predominant ABFR in majority of the
investigated species (Chinese bitterling, crucian carp, tilapia, shrimp
and dragonfly larvae), with mean contributions of 53%–90% to
∑ABFRs. The result may indicate that DBDPE was the major ABFRs in
the environment of the e-waste recycling site; this is consistent with
previous reports (Zheng et al., 2015; Hong et al., 2018; Liu et al.,
2018b). However, in northern snakehead and mud carp, HBB made the
greatest contribution to ∑ABFRs (accounting for > 70% of ∑ABFRs). A
high proportion of HBB was also observed in northern snakehead and
mud carp previously collected from the same e-waste recycling site
which includes the present sampling site (Wu et al., 2010). The log n-
octanol/water partition coefficient (KOW) of HBB is 6.11 (EFSA, 2012),
which falls into the optimum range for biomagnification (Kelly et al.,
2007). This may contribute to elevated HBB levels in organisms at high
trophic levels, such as northern snakehead and mud carp (Wu et al.,
2010). PBT and PBEB collectively constituted < 10% of ∑ABFRs in all
samples and were regularly reported in relatively low amounts in
aquatic organisms from the e-waste area in South China (Liu et al.,
2018a, 2018b; Zheng et al., 2012). Interestingly, BTBPE was found to
be the major ABFR (accounting for 77% of ∑ABFRs) in water beetles.
L. Tao, et al. Environment International 127 (2019) 226–232

Table 1
Levels (ng/g lw) of measured ABFRs of the predator fish and the candidate prey collected from an e-waste recycling sitea.
NS (n = 15) MC (n = 18) CB (n = 6) CC (n = 7) TIA (n= 9) SHP (n = 7)b DL (n = 3)b WB (n = 3)b

Lip % dw 1.96 ± 0.17c 18.6 ± 1.47 8.12 ± 0.49 7.33 ± 0.89 9.46 ± 0.51 5.17 ± 0.24 3.53 ± 0.25 13.4 ± 1.90

ABFRs
DBDPE 141 ± 44.2 233 ± 52.7 79.9 ± 27.1 1700 ± 744 11,800 ± 4400 823 ± 268 25,400 ± 5020 77.4 ± 21.0
BTBPE 114 ± 28.0 160 ± 52.5 11.7 ± 1.38 273 ± 128 245 ± 130 162 ± 60.1 721 ± 149 466 ± 216
HBB 598 ± 111 672 ± 49.3 46.0 ± 11.6 795 ± 185 1330 ± 691 118 ± 65.3 1760 ± 315 16.5 ± 6.45
PBT 9.24 ± 1.50 3.32 ± 0.43 1.63 ± 0.38 4.10 ± 0.81 28.5 ± 13.3 4.35 ± 1.29 33.0 ± 15.2 0.77 ± 0.23
PBEB 36.0 ± 6.70 12.0 ± 1.44 2.47 ± 0.17 15.4 ± 5.43 35.9 ± 4.06 18.2 ± 1.63 29.0 ± 7.62 27.1 ± 2.87
∑ABFRsd 874 ± 146 1080 ± 126 128 ± 28.0 2670 ± 736 13,500 ± 4220 1010 ± 248 28,000 ± 4850 590 ± 240

PBDEs
BDE 28 830 ± 120 1510 ± 100 33.9 ± 8.41 692 ± 219 460 ± 55.2 373 ± 44.6 216 ± 82.8 75.0 ± 25.0
BDE 47 6080 ± 997 4900 ± 508 241 ± 43.7 5080 ± 1115 2700 ± 285 3080 ± 388 934 ± 184 25.0 ± 7.55
BDE 66 66.7 ± 12.2 30.4 ± 4.94 3.80 ± 0.46 61.6 ± 26.9 113 ± 16.8 92.9 ± 7.53 98.9 ± 27.6 109 ± 23.2
BDE 99 42.1 ± 17.5 14.1 ± 1.54 12.2 ± 2.35 93.6 ± 52.3 1100 ± 121 266 ± 21.1 426 ± 90.8 195 ± 7.20
BDE 100 1000 ± 146 765 ± 81.1 33.2 ± 9.07 776 ± 163 445 ± 28.3 431 ± 58.0 181 ± 39.4 ND
BDE 138 138 ± 36.4 161 ± 28.0 6.15 ± 0.36 107 ± 19.6 273 ± 47.7 132 ± 9.80 158 ± 60.2 34.8 ± 6.66
BDE 153 259 ± 42.6 901 ± 99.2 23.0 ± 5.77 663 ± 202 1880 ± 163 248 ± 26.6 540 ± 94.3 266 ± 64.5
BDE 154 1380 ± 176 2380 ± 264 51.4 ± 11.0 960 ± 220 1240 ± 92.0 370 ± 62.8 203 ± 31.5 19.3 ± 1.16
BDE 183 28.7 ± 5.39 29.3 ± 4.89 5.22 ± 1.13 61.0 ± 18.8 121 ± 26.8 52.8 ± 8.54 326 ± 38.0 57.0 ± 3.65
BDE 196 33.3 ± 5.32 29.3 ± 22.2 13.6 ± 1.69 19.0 ± 6.21 68.3 ± 14.8 15.0 ± 3.70 232 ± 34.4 20.3 ± 2.70
BDE 197 50.5 ± 8.65 11.7 ± 1.97 18.4 ± 1.86 27.0 ± 8.09 84.4 ± 16.7 30.5 ± 6.09 230 ± 34.5 29.0 ± 5.96
BDE 202 140 ± 26.6 122 ± 84.4 15.7 ± 1.96 37.0 ± 11.1 115 ± 22.6 41.8 ± 8.33 315 ± 47.2 40.4 ± 7.49
BDE 203 30.4 ± 4.93 23.7 ± 16.0 12.6 ± 1.31 21.9 ± 6.72 75.1 ± 14.2 19.1 ± 4.54 231 ± 33.9 23.1 ± 5.09
BDE 206 117 ± 14.8 35.3 ± 7.66 49.3 ± 7.44 171 ± 70.5 730 ± 198 138 ± 57.1 2954 ± 544 24.5 ± 0.65
BDE 207 35.8 ± 13.4 81.6 ± 46.4 30.3 ± 10.3 106 ± 46.2 533 ± 148 86.7 ± 35.5 1690 ± 78.1 49.3 ± 0.77
BDE 208 17.6 ± 7.23 19.2 ± 5.42 15.8 ± 5.80 53.6 ± 22.5 318 ± 83.1 63.9 ± 20.9 940 ± 8.17 30.3 ± 4.10
BDE 209 1410 ± 365 1120 ± 227 555 ± 71.3 11,700 ± 6940 40,000 ± 14,800 4380 ± 264 138,000 ± 16,400 525 ± 11.9
∑PBDEse 11,600 ± 1770 12,000 ± 1040 1120 ± 108 20,600 ± 8020 50,300 ± 14,300 9200 ± 816 147,000 ± 16,600 1520 ± 34.1

a
NS, northern snakehead (Channa argus); MC, mud carp (Cirrhinus molitorella); CB, Chinese bitterling (Rhodeinae); CC, crucian carp (Carassius auratus); TIA, tilapia
(Oreochromis spp); SHP, shrimp (Neocaridina denticulata); DL, dragonfly larvae (Aeshnidae rambur); WB, water beetle (Sternolophus inconspicuus).
b
Number of pooled samples when individuals were pooled.
c
Mean ± SE.
d
Sum concentrations of the 5 ABFRs examined.
e
Sum concentrations of 18 PBDE congeners (BDEs 28, 47, 66, 85, 99, 100, 138, 153, 154, 183, 196, 197, 202, 203, 206, 207, 208, and 209).

Fig. 1. Concentration ratios of ∑ABFRs to ∑PBDEs in northern snakehead and

its potential prey from an e-waste recycling site in South China. Error bars
represent ± 1SE. NS, northern snakehead (Channa argus); MC, mud carp
(Cirrhinus molitorella); CB, Chinese bitterling (Rhodeinae); CC, crucian carp
(Carassius auratus); TIA, tilapia (Oreochromis spp); SHP, shrimp (Neocaridina
denticulata); DL, dragonfly larvae (Aeshnidae rambur); WB, water beetles
(Sternolophus inconspicuus).
The data are lacking for BTBPE concentrations in insects; and the un-
ique ABFR profile found in water beetles in our study cannot be ade-
quately explained based on the existing data.
3.2. FA compositions and the dietary composition of northern snakehead
A summary of FA compositions in northern snakehead and its po-
tential prey species is listed in Table S1 in the Supplementary Data. The
Fig. 2. Profiles of AHFRs in northern snakehead and its potential prey from an
e-waste recycling site in South China.
proportions of saturated FAs (SFAs), monounsaturated FAs (MUFAs),
and polyunsaturated FAs (PUFAs) contributed to 30%–52%, 15%–48%,
and 15%–38% to the total FAs, respectively. In fish and shrimp samples,
FAs 16:0 and 18:1n-9 were typically the most abundant SFA and MUFA,
respectively; which is in agreement with previous reports on FA com-
positions in freshwater fish and shrimp (Rodrigues et al., 2017; Li et al.,
2011). For PUFAs, FA 22:6n-3 was predominant in northern snakehead,
Chinese bitterling, and crucian carp, while 18:2n-6 and 20:5n-3 were
the major FAs in mud carp and shrimp, respectively. Additionally, in
the present study, northern snakehead and crucian carp had relatively
high levels of total n-3 PUFAs. They even displayed higher

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L. Tao, et al. Environment International 127 (2019) 226–232

Table 2
Contributions of each diet items to the total diet of northern snakehead (NS) individuals, estimated based on FA signatures.
NS individual MC CB CC TIA SHP DL WB

a b
NS1 TA TA 87.4 ± 1.16 % TA 12.6 ± 1.30% TA TA
NS2 17.8 ± 0.12% TA 82.2 ± 0.66% TA TA TA TA
NS3 TA TA 84.1 ± 1.81% TA 15.9 ± 1.35% TA TA
NS4 TA TA 73.7 ± 1.21% TA 26.3 ± 1.04% TA TA
NS5 TA TA 85.3 ± 1.25% TA 14.7 ± 1.39% TA TA
NS6 TA TA 81.0 ± 1.12% TA 19.0 ± 1.28% TA TA
NS7 TA TA 71.3 ± 1.34% TA 28.7 ± 1.35% TA TA
NS8 TA TA 71.4 ± 1.89% TA 28.5 ± 1.22% TA TA
NS9 TA TA 99.9 ± 0.94% TA 0.03 ± 0.88% TA TA
NS10 TA TA 70.0 ± 1.95% TA 30.0 ± 1.52% TA TA
NS11 TA TA 100 ± 0.85% TA 0.02 ± 0.79% TA TA
NS12 0.01 ± 0.05% TA 93.5 ± 1.05% TA 6.52 ± 1.08% TA TA
NS13 TA TA 99.6 ± 1.04% TA 0.37 ± 0.80% TA TA
NS14 TA TA 100 ± 0.95% TA TA TA TA
NS15 TA TA 99.6 ± 1.07% TA 0.40 ± 0.95% TA TA
Mean ± SE 1.19 ± 1.18% TA 86.6 ± 3.00% TA 12.2 ± 3.11% TA TA

a
TA: Trace amount (< 0.01%).
b
SE for each pk was calculated as mentioned in the SI.

concentrations of 20:5n-3 (eicosapntemacnioc acid, EPA) and 22:6n-3
(docosahexaenoic acid, DHA), two nutritionally important FAs, as
compared to some marine fishes (Li et al., 2011; Osman et al., 2001;
Tanakol et al., 1999). For the two insect species studied, dragonfly
larvae and water beetles, FAs 16:0, 18:0, 18:1n-9, and 18:2n-6 were the
major FAs. Unlike fish and shrimp, the insect species showed small
fractions of DHA, indicating unique FA profiles in the insects.
A total of 16 of the 37 FAs were selected and normalized to 100%
(Table S2 in the Supplementary Data). Based on the FA signatures in the
predator and its forage species, we estimated the contribution of each
prey type to the total diet of northern snakehead (Table 2). Crucian carp
was found to be the main prey of northern snakehead, with contribu-
tions of 71%–100% to the total diet. Shrimp was another main food
source for the northern snakehead, with a maximum proportion up to
30%. In two individual northern snakehead, mud carp also contributed
small fractions (17.8% and 0.01%) to the total diet (Table 2).
3.3. Biomagnification factors of ABFRs
The BMFFA of ABFRs are illustrated in Fig. 3. PBT and PBEB showed
BMFFA values higher than 1 (2.09 and 2.13, respectively), indicating
their significant biomagnification in northern snakehead. In contrast,
DBDPE, BTBPE, and HBB were subjected to trophic dilution, with mean
BMFFA values of 0.06, 0.40, and 0.91, respectively.
Fig. 3. BMFFA values for ABFRs compared with PBDEs. Error bars
represent ± 1SE. The red line represents BMFFA = 1. (For interpretation of the
references to colour in this figure legend, the reader is referred to the web
version of this article.)
Although we determined the BMF values for ABFRs based on the
diet composition of the predator, various factors contribute to the un-
certainties in their values. Abundance of the various prey species in the
pond might affect both the species of fish and ABFRs consumed by
northern snakeheads, in turn influencing the biomagnification of the
ABFRs. Additionally, the levels of ABFRs were determined using the
dorsal muscle of the predator, while entire organism was used as a
sample for its potential prey, which may cause potential biases in the
estimated BMFFAs. It is likely that the levels of ABFRs in the dorsal
muscle of fish are lower than those estimated from the entire organism.
Based on the literatures (Gandhi et al., 2017; Stone, 2006), a factor of
2–5 might be expected between whole-body and muscle concentrations
of PBDEs in fish. Thus, the current BMFFA may be 2–5 times under-
estimated. Further investigations including the trophic ecology of
northern snakehead are warranted to fully understand the biomagnifi-
cation potentials of these emerging chemicals.
To date, no BMFFA values of ABFRs are available for comparison.
High biomagnification potential for PBDEs has been reported in aquatic
biota (Munschy et al., 2017; Zheng et al., 2016). The BMFFA values for
PBDE congeners were also calculated in the same northern snakehead
individual for comparison (Fig. 3). The BMFFAs for PBT and PBEB were
higher than those for majority of the PBDE congeners. The BMFFA for
HBB was comparable to those for BDEs 28, 47, 66, 100, 138, 154, and
206, but was significantly greater than those for BDEs 99, 153, 183,
207, 208, and 209 (t-test, p < 0.05). These results suggested that some
ABFRs such as PBT, PBEB, and HBB have comparable or even higher
biomagnification potentials relative to PBDEs.
It was suggested that the n-octanol/water partition coefficients
(KOW) of a hydrophobic organic pollutant is an important factors in
regulating its biomagnification (Kelly et al., 2007). In the present study,
a significant and negative correlation between the BMFFA values of
ABFRs and PBDEs and the log KOWs of these chemicals was observed
(Fig. 4; r = −0.65, p = 0.002). Most of the chemicals examined in the
present study possess a log KOW > 7. Previous studies demonstrated
that the biomagnification potential of hydrophobic organic pollutants
with log KOWs > 7 in aquatic biota generally decreases with the in-
creasing log KOW values (Kelly et al., 2007; Burreau et al., 2004; Hu
et al., 2010). The decrease in BMFs is likely due to their reduced uptake
efficiency, biodegradation in vivo, and potentially inaccurate KOW es-
timates for these superhydrophobic chemicals (Kelly et al., 2007;
Burreau et al., 2004).
4. Conclusions
This study is the first to estimate BMFs for ABFRs based on

230
L. Tao, et al.
Fig. 4. Correlation of BMFFA for ABFRs and PBDEs with the log KOWs of these
chemicals. The log KOW values of ABFRs and PBDEs were from EFSA (2012) and
deBruyn et al. (2009), respectively.
quantitative determination of the dietary composition of a predator.
Our results showed that the widely used ABFR, DBDPE, does not seem
to biomagnify in the predatory fish studied. However, some ABFRs such
as PBT and PBEB biomagnified, with comparable biomagnification
potentials to PBDEs that are no longer in use. Thus, some ABFRs may
pose significant risks to aquatic organisms in habitats where the use of
these contemporary flame retardants is still prevalent.
Acknowledgments
Mr. Shu-Ming Fang from the GIGCAS is kindly acknowledged for his
assistance in the estimation of diet composition of the predator. This
work was financially supported in part by the National Natural Science
Foundation of China (Grant 41373105), the Strategic Priority Research
Program of the Chinese Academy of Sciences (Project XDB14020301),
and the National Basic Research Program of China (Project
2015CB453102). Bi-Xian Mai is grateful to the Local Innovative and
Research Teams Project of Guangdong Pearl River Talents Program
(grant 2017BT01Z134) and the Key Research Program of Frontier
Sciences, CAS (grant QYZDJ-SSW-DQC018) for financial support.
Appendix A. Supplementary data
Supplementary data to this article include contaminant analysis, FA
analysis, estimation of the dietary composition of northern snakehead,
and Tables S1 and S2. Supplementary data to this article can be found
online at doi: https://doi.org/10.1016/j.envint.2019.03.036.
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