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Keywords:

  • Polybrominated diphenyl ethers (PBDEs);
  • Polychlorinated biphenyls (PCBs);
  • Biomagnification;
  • Fish size;
  • Molecular size

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs), two types of persistent organic pollutants that have been used widely, can be released into the environment and accumulate in organisms. To obtain a better understanding of the biomagnification of PBDEs and PCBs in fish, as well as the influences on biomagnification by fish size and physical properties of PBDEs and PCBs, a total of 200 samples of 24 fish species were collected and analyzed from Taihu Lake, the second largest freshwater lake in China. The concentrations of PBDEs and PCBs ranged from 8.59 to 74.28 ng/g lipid weight (lw) and from 10.30 to 165.20 ng/g lw, respectively. Trophic magnification factors (TMFs) were used to estimate the PBDE and PCB biomagnification potentials. The TMF values of PBDEs and PCBs ranged from 0.78 to 2.95 and from 0.92 to 2.60, respectively. Most of the TMFs were greater than 1, indicating that these contaminants were biomagnified in food chains. Fish size might influence the biomagnification evaluation, because different sized fish had different lipid content, leading to different lipid-based concentrations of PBDEs and PCBs. Parabolic relationships were observed between the TMFs and logKOW, as well as between the TMFs and the molecular volumes of PBDE and PCB congeners. The congeners with logKOW values of approximately 7 or molecular volumes of approximately 8 × 10−5 nm3 had the greatest biomagnification potentials. Compared to molecular weight, molecular volume seems to be the better standard for analyzing the influence of molecular size on biomagnification. Environ. Toxicol. Chem. 2012;31:542–549. © 2011 SETAC


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs), two types of persistent organic pollutants used in household plastic products, electronic goods, and many industrial products, can be released into the environment and are now ubiquitously present. These compounds are of great concern because of their persistence and adverse effects on organisms 1, 2. Polychlorinated biphenyls have been listed as priority-controlled contaminants. Penta- and octa-BDE products were nominated as new priority-controlled contaminants listed in Annex A of the Stockholm Convention on persistent organic pollutants in 2009 3.

Because of their persistence and high lipophilicity, PBDEs and PCBs are capable of undergoing long-range transport, bioconcentration, and biomagnification through food chains 4–7. Trophic magnification factor (TMF), which represents the average increase rate per trophic level, can be used to indicate the biomagnification potentials of hydrophobic organic compounds (HOCs) 8–10. Many factors, such as the length and structure of food chains, the investigated species (e.g., poikilotherms and homoiotherms), the environmental conditions (e.g., temperature), and the contamination levels can affect HOC biomagnification. For example, longer food chains are expected to have higher biomagnification potentials for PBDEs 7, 11, water temperature can affect the metabolism capacity of an organism and thus biomagnification, and more efficient digestion of food can lead to greater biomagnification potentials of nonmetabolizable substances 12.

Until now, investigations of the TMFs of PBDEs and PCBs in freshwater food chains have been limited 6, 7, 13–15. Most of the TMFs of PBDEs reported in the literature were obtained from highly PBDE-contaminated freshwater systems 7, 15. Only a few studies have been performed in slightly PBDE-contaminated freshwater systems 6, 16. In addition, the influences of fish size and physical properties of HOCs (especially molecular size) on biomagnification are still not well understood 17, 18, although factors such as the growth of species and physiochemical properties of chemicals (for example, molecular size and octanol-water partition coefficient [KOW]) have been reported to affect biomagnification 7, 10.

Taihu Lake, the second largest freshwater lake in China, is located in the Jiangsu Province and is surrounded by important agricultural areas. Rapid industrial development has occurred around the lake since the 1980s because of an economic boom. As a result, the water in the lake has been deteriorating and many HOCs, such as organochlorine pesticides, PCBs, and PBDEs, have been detected 19–22. However, so far, the PBDE levels in fish, as well as the biomagnification of PBDEs and PCBs in food chains from Taihu Lake, have not been reported.

Toxicity, environmental persistence, bioaccumulation, and trophic transfer of PBDEs and PCBs in aquatic ecosystems are vital for assessing the ecological risk of the contaminants and human health risk via fish consumption. Therefore, the first objective of the present study is to investigate the levels and composition profiles of PBDEs and PCBs in fish from Taihu Lake. The second objective is to investigate the biomagnification of the contaminants, in particular, the influence of fish size and physical properties (especially molecular size) of the contaminants on biomagnification.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

Sampling and sample preparation

Taihu Lake (30°55′-31°33′N, 119°55′-120°36′E) is situated in the south of the Yangtze Delta in mid-eastern China, with a land area of 2,338 km2 and an average water depth of 1.9 m. Fish were caught by commercial fishers from Taihu Lake in September 2009. A total of 200 samples of 24 fish species were collected, including three types of herbivorous fish: Ctenopharyngodon idellus, Megalobrama amblycephala, and Parabramis pekinensis; 10 types of omnivorous fish: Carassius carassius, Cyprinus carpio, Hypophthalmichthys molitrix, Hemiculter leucisculus, Acheilognathus macropterus, Hypophthalmichthys nobilis, Saurogobio dabryi, Hyporhamphus intermedius, Pelteobagrus fulvidraco, and Toxabramis swinhonis; and 11 types of carnivorous fish: Coilia ectenes taihuensis, Hemibarbus maculates, Cultrichthys erythropterus, Culter alburnus, Protosalanx hyalocranius, Neosalanx taihuensis Chen, Chanodichthys mongolicus, Chanodichthys dabryi, Paracanthobrama guichenoti, Silurus asotus, and Acheilognathus rhombeus. The collected fish were stored in ice, transported to the laboratory immediately, then stored at −18°C until use. After measuring the length and weight of each individual fish, they were thawed and filleted. The fillets were homogenized and lyophilized to dryness, ground into powders, and stored in clean amber glass containers at −18°C until use. Detailed information is given in the Supplemental Data, Table S1.

Analyses

Concentrations of PBDE and PCB, as well as lipid content, were determined with a method described in our previous study 23. Briefly, the lyophilized samples (8 g) spiked with the surrogate standard 13C-PCB141 (4 ng) (Cambridge Isotope Laboratories) were extracted in a Soxhlet extractor for 72 h. Lipid content of the samples was determined gravimetrically using 25% of the extracts (Supplemental Data, Table S1). The remaining extracts were purified by gel permeation chromatography and multilayer silica-alumina column chromatography. The internal standard 13C-PCB208 (1 ng) (Cambridge Isotope Laboratories) was added to the concentrated eluates. The final volumes of the samples were 50 µL. All samples were stored at −18°C until analyses by using gas chromatograph-mass spectrometer. Detailed information is given in the Supplemental Data.

The stable isotope ratio analyses for nitrogen in fish tissues were performed on an elemental analyzer-isotope ratio mass spectrometer (DELTAplus XL, Thermo Finnigan MAT). Typically, the fish tissues (1 mg) were weighed in tin capsules, which were dropped into a CuO combustion furnace in a CE EA1112 C/N/S analyzer through an autosampler and combusted at 960°C in an oxygen atmosphere. The stable isotope ratios of nitrogen were measured in the DELTAplus XL mass spectrometer coupled to a CE EA1112 C/N/S analyzer through a Conflo III interface (Finnigan). The stable isotope ratios of nitrogen, which are given as parts per thousand deviations from standards, were calculated as follows:

  • equation image(1)

where R is 15N/14N.

The molecular diameters and volumes of PBDE and PCB congeners were calculated as follows. The geometric structures of PBDE and PCB congeners were optimized via semiempirical molecular orbital method PM3, and then the molecular diameters and volumes were calculated by using a quantitative structure–activity relationship model. In this study, the molecular diameter is defined as the largest distance of two atoms in a molecule.

Calculations

The trophic level (TLconsumer) was determined relative to zooplankton (which was assumed to occupy a trophic level of 2) by using the following equation 24

  • equation image(2)

where δ15Nzooplankton of 14.9‰ in Taihu Lake was used according to the results reported by Zhou et al. 25, and 3.4 is the isotopic enrichment factor 26.

The biomagnification potentials of PBDE and PCB congeners in food chains were quantified by TMFs, which were derived from the slopes of lipid-normalized concentrations of the contaminants versus trophic levels of the species 9

  • equation image(3)

where k and b are the empirical slope and y intercept, respectively, and CL is the lipid-normalized concentration of an individual PBDE or PCB congener.

Quality assurance and quality control

A procedural blank was run for each batch of six samples to monitor all interference during sample extraction and the following treatment. The values obtained from the blanks were subtracted from the samples. Seven working solutions of the PBDE standard, including 14 PBDE congeners (i.e., BDE17, 28, 47, 66, 71, 85, 99, 100, 138, 153, 154, 183, 190, and 209), and the PCB standard, including 39 PCB congeners (i.e., PCB1, 2, 3, 4, 6, 8, 9, 16, 18, 19, 22, 25, 28, 44, 52, 56, 66, 67, 71, 74, 82, 87, 99, 110, 138, 146, 147, 153, 173, 174, 177, 179, 180, 187, 194,195, 199, 203, and 206) in iso-octane were used. The reported concentrations were not corrected against the recovery rate of the surrogate standard 13C-PCB141, which varied from 79.5% to 126.5%, with an average of 97.9 ± 10.0%. The limits of detection ranged from 25 to 75 pg/g lipid weight (lw) for tri- to hepta-BDEs and 300 pg/g lw for BDE209, and from 33.3 to 216.7 pg/g lw for PCBs, which were calculated according to 3.36 times the standard deviation of the PBDE and PCB concentrations, with approximately 5 times the signal-to-noise ratio.

For the δ15N analyses, the standards with the δ15N at 6.70‰ were analyzed to evaluate the reproducibility and accuracy of the instrument at the beginning and end of each batch of sample analyses (usually 10 samples).

Statistical analysis

The statistical analyses of data were carried out by using SPSS 11.5 for Windows. The relationships between the TMFs and the parameters (i.e., logKOW, molecular weight, and molecular volume) were analyzed by using quadratic estimation. It was considered statistically significant when p < 0.05. When the amount of a congener was lower than its limits of detection, its concentration was reported as zero.

RESULTS AND DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

Levels and composition profiles of PBDEs and PCBs

The total concentrations of PBDEs and PCBs in each species are listed in Table 1. The average total concentrations of PBDEs and PCBs in each species ranged from 8.6 to 74.3 ng/g lw and from 10.3 to 165.2 ng/g lw, respectively. The lowest and highest concentrations of PBDEs and PCBs were observed in S. dabryi and S. asotus, respectively. Compared with those in wild freshwater fish in other studies in China (Supplemental Data, Table S2), the fish in Taihu Lake are only moderately contaminated by PBDEs and PCBs.

Table 1. Total concentrations (ng/g lipid wt) of PBDEs and PCBs, the stable nitrogen isotope, and trophic levels of fish species collected from Taihu Lake, China
Speciesnaδ15NbTLPBDEsPCBs
Mean (median)RangeMean (median)Range
  • a

    n = the number of the samples of the species.

  • b

    Arithmetic mean ± standard deviation.

    TL = trophic level; PBDE = polybrominated diphenyl ethers; PCB = polychlorinated biphenyls.

Herbivorous fish
 Ctenopharyngodon idellus411.7 ± 0.51.0610.57 (8.7)5.4–19.521.6 (20.7)20.3–24.8
 Megalobrama amblycephala616.0 ± 1.82.3225.86 (23.0)20.1–40.738.0 (26.4)20.1–88.8
 Parabramis pekinensis419.7 ± 4.83.4030.48 (29.7)15.7–46.987.1 (90.9)57.1–109.7
Omnivorous fish
 Carassius carassius1818.3 ± 1.73.0118.60 (17.1)11.6–39.748.9 (46.8)30.8–76.7
 Cyprinus carpio1117.6 ± 1.62.7914.74 (13.0)8.6–31.438.7 (37.5)24.7–59.8
 Hypophthalmichthys molitrix1216.9 ± 1.02.5941.22 (23.5)8.5–99.445.6 (43.4)18.0–100.2
 Hemiculter leucisculus616.7 ± 1.02.5264.13 (27.1)11.7–265.937.7 (34.1)20.1–58.6
 Acheilognathus macropterus815.0 ± 3.42.029.25 (6.9)5.5–19.118.5 (9.8)7.9–52.7
 Hypophthalmichthys nobilis1016.6 ± 1.82.5126.77 (20.1)8.7–53.065.9 (61.2)41.2–97.3
 Saurogobio dabryi217.32.718.597.1–10.110.39.8–10.8
 Hyporhamphus intermedius716.4 ± 0.62.4530.26 (32.1)10.8–49.324.0 (24.0)22.5–26.2
 Pelteobagrus fulvidraco1218.8 ± 1.83.1430.86 (29.4)14.1–53.472.0 (68.0)32.5–118.3
 Toxabramis swinhonis416.6 ± 0.92.5140.84 (40.7)40.2–41.740.8 (39.9)32.7–50.8
Carnivorous fish
 Coilia ectenes taihuensis2919.5 ± 1.73.3526.89 (23.3)7.2–57.540.4 (35.3)17.1–87.1
 Hemibarbus maculatus919.5 ± 1.23.3515.43 (14.8)11.8–20.633.6 (31.9)20.2–69.3
 Cultrichthys erythropterus1419.9 ± 1.03.4732.15 (30.9)20.6–54.893.4 (84.5)60.2–150.2
 Culter alburnus1119.7 ± 1.23.3524.69 (21.5)16.1–40.577.5 (77.3)53.2–116.5
 Protosalanx hyalocranius917.0 ± 1.62.6140.81 (44.1)22.4–53.074.8 (73.2)32.4–120.7
 Neosalanx taihuensis Chen917.0 ± 1.42.6233.35 (32.8)25.2–47.647.4 (45.6)41.0–53.8
 Chanodichthys mongolicus717.6 ± 1.92.8010.31 (10.6)7.6–13.534.5 (29.6)24.3–50.5
 Chanodichthys dabryi314.8 ± 0.81.9720.18 (20.0)15.7–24.836.7 (36.3)29.6–44.1
 Paracanthobrama guichenoti217.12.6426.0418.4–33.733.327.4–39.2
 Silurus asotus219.83.4574.2861.4–87.1165.2145.2–185.2
 Acheilognathus rhombeus118.43.0428.6428.6–28.644.044.0–44.0

The concentrations of individual PBDE and PCB congeners are listed in Supplemental Data, Table S2. Polybrominated diphenyl ethers and PCBs were detected in all samples with BDE47, 209, and 154, with PCB153, 138, and 28 being the most abundant congeners, respectively. In all, BDE47 accounted for 10.8 to 52.7% of the total PBDEs (Supplemental Data, Fig. S1). The major contribution of BDE47 rather than BDE99 to total PBDEs in the species is consistent with results reported in the literature 8, 16. Metabolism of highly brominated BDEs (e.g., BDE99) in fish may be responsible for this observation because BDE47 is not the most abundant congener in technical PBDE products 27, 28. In addition, the high bioavailability of BDE47 may be another important reason. Qiu et al. 22 reported that the predominant congeners in the air in Taihu Lake were BDE209, followed by BDE47. The relative abundance of tetra- and tri-BDE congeners (including BDE47, 28, 49, 66, and 17) instead of BDE99 indicates that a specific penta-BDE formulation might be produced or consumed in this region 22. This specific formulation was also proposed as the source of PBDEs in human milk in the regions around Taihu Lake 29.

In all, BDE209 accounted for 3.7 to 69.6% of the total PBDEs. The presence of BDE209 in fish indicates that it can be taken up by organisms, thus demonstrating its bioavailability as reported in the literature 4, 5, 30. In herbivorous and omnivorous fish (except for P. pekinensis), the contribution of BDE209 to the total PBDEs was high, ranging from 15.0 to 69.6%, with an average of 38.3%. In contrast, in carnivorous fish, the contribution varied between 3.7 and 19.7%, with an average of 10.3%. We speculated that this phenomenon might be related to the sediment-associated particles and the metabolism of BDE209 in the species. Shaw et al. 31 proposed that marine fish accumulates BDE209 via ingestion of sediment-associated organisms such as zooplankton and benthic invertebrates.

The high levels of BDE154, especially in carnivorous fish, may be attributed to metabolism of highly brominated BDEs (e.g., BDE209), because carnivorous fish are in a high trophic position, and fish in a higher trophic position have an increased metabolism capability 9, 32. Our data are consistent with this speculation. In carnivorous fish, BDE154 accounted for 7.0 to 40.8% of the total PBDEs, with an average of 18.5%, which is much higher than its percentage in technical PBDE products (5.3–8.7%) 27. In contrast, the contribution of BDE154 to total PBDEs in herbivorous and omnivorous fish ranged from 5.0 to 17.9%, with an average of 10.1% (Supplemental Data, Fig. S1). The observations also support the speculation of the BDE209 metabolism in carnivorous fish as aforementioned.

For the PCBs measured, PCB153, one of the most recalcitrant PCB congeners with respect to biotransformation 33, was the most abundant congener, accounting for 12.1 to 24.9% of the total PCBs, followed by PCB138 (6.8–19.1%) and PCB28 (2.8–9.6%) (Supplemental Data, Fig. S1). Hexa-PCBs contributed to the largest proportion of the total PCBs, followed by tetra- and penta-PCBs. Combined octa- and nona-PCBs accounted for an average of 4.1% of the total PCBs. Elevated proportions of lowly halogenated congeners suggest the occurrence of dehalogenation of highly halogenated congeners and confirmed the prevalence of biotransformation of these compounds in fish 6, 33.

Trophic magnification factor

Biomagnification can be monitored by the stable nitrogen isotope of organism tissues, because organisms at higher trophic levels in food chains enrich the heavier isotope of nitrogen. According to Equation 2, the trophic levels of the species ranged from 1.06 to 3.47 (Table 1). Linear relationships were found between the trophic levels and lipid-based concentrations of PBDE and PCB congeners. Representative relationships between the trophic levels and the BDE47 and PCB153 concentrations are shown in Figure 1. The TMFs of individual PBDE and PCB congeners are calculated using Equation 3. The TMFs of PBDEs and PCBs ranged from 0.78 (BDE209) to 2.95 (BDE100) and from 0.92 (PCB16) to 2.60 (PCB146), respectively (Table 2). Usually, a TMF value greater than 1 indicates the presence of biomagnification of the chemical through a food chain 9. Therefore, the present TMFs indicate that the significant biomagnification of most of PCBs and some of PBDEs in the surveyed food chains had occurred (Table 2).

thumbnail image

Figure 1. Relationships between the polychlorinated biphenyl (PCB)153 and brominated diphenyl ether (BDE) 47 concentrations and trophic levels of the species. The filled and open spots represent PCB153 and BDE47, respectively.

Download figure to PowerPoint

Table 2. Molecular diameter and molecular volume of PBDE and PCB congeners, and TMFs and the significance (p values) for the congeners through the food chain in Taihu Lake, China
CongenerMD (0.1nm)MV (10−3nm3)TMFp valueaCongenerMD (0.1nm)MV (10−3nm3)TMFp valuea
  • a

    The significance for the relationships between the lipid-normalized concentrations of the congeners and trophic levels.

    PBDE = polybrominated diphenyl ethers; PCB = polychlorinated biphenyls; TMF = trophic magnification factor; MD = molecular diameter; MV = molecular volume.

PBDEs
 BDE1710.88714.961.390.243BDE15410.47892.001.870.026
 BDE2811.34740.141.490.072BDE15310.43902.272.140.043
 BDE4711.60770.681.970.001BDE13811.67881.440.910.873
 BDE6611.28782.651.830.133BDE18310.55934.790.960.933
 BDE10011.76844.472.950.004BDE19011.65926.411.880.285
 BDE9910.47853.921.590.204BDE20911.821051.930.780.475
 BDE8511.62856.131.700.499     
PCBs
 PCB199.46653.231.230.700PCB829.93731.862.300.003
 PCB189.36661.571.390.075PCB14710.05771.252.44<0.001
 PCB169.35656.670.920.819PCB1469.94779.862.60<0.001
 PCB259.89669.071.290.368PCB15310.51779.271.870.003
 PCB2810.46669.551.340.112PCB1799.70799.892.18<0.001
 PCB229.89664.551.270.297PCB13810.51774.951.840.003
 PCB529.36703.541.370.093PCB18710.05808.102.43<0.001
 PCB449.36698.891.800.007PCB17410.05804.191.830.069
 PCB719.94699.572.330.010PCB17710.05803.912.45<0.001
 PCB679.89707.101.040.740PCB17310.05799.771.850.057
 PCB7410.46707.202.070.001PCB18010.51811.762.030.030
 PCB6610.46707.091.980.003PCB19910.05841.581.830.120
 PCB569.89702.571.400.251PCB20310.62841.761.930.053
 PCB9910.50741.512.58<0.001PCB19510.61836.872.180.109
 PCB879.94736.642.240.001PCB19410.51844.992.360.042
 PCB1109.94736.812.150.008PCB20610.62875.761.560.059

Similar biomagnification of PBDEs and PCBs has been widely reported in both marine and freshwater food chains. Compared with the results in the literature (Supplemental Data, Table S4), the TMFs of PBDEs and PCBs in the present study fell in the range of the reported TMF values from both freshwater and seawater food chains. As mentioned in the Introduction, many factors, such as the lengths and structures of food chains, the investigated species, the environmental conditions, the levels of contaminants, the other biological factors, and physiochemical properties, could influence the biomagnification of HOCs. The present data may reflect the combined results of the factors.

Influence of fish size on biomagnification

Two variables, that is, the length and body weight of fish, can be used to investigate the effect of fish size on biomagnification 4, 5, 18. Because of the limited number of samples or small variations in length within the same species, only seven species with length ratios (i.e., longest to the shortest length within the same species) higher than 1.5 and sample numbers higher than five were used to analyze the relationships. Because the fish length varied within narrow ranges in a given species and the B values ranged from 2.5 to 3.3 (Table 3), the relationship between body weight and fish length could be linearly regressed, with an R2 of 0.875 to 0.974 and all p values <0.001 (Supplemental Data, Table S5). As a result, using either body weight or fish length to examine the influence of the fish size on the biomagnification of PBDEs and PCBs would make no difference. However, unlike body weight, fish length is not influenced by the fed status of fish. Therefore, in the present study, we used fish length to examine the effects of fish size on biomagnification. The lipid contents (%, w/w) and the concentrations of PBDEs and PCBs were linearly regressed against fish length, and the results are listed in Table 3.

Table 3. The parameters of the regression equations of the relationships between the length and the body weight, lipid content, and concentrations of PBDEs and PCBs
Species PBDEs
Weight-lengthaCWet-lengthb,dCLipid-lengthb,e
ABR2kR2pkR2P
Coilia ectenes taihuensis0.02232.470.9580.0650.1850.058−1.9700.2850.015
Cultrichthys erythropterus0.00593.260.9970.0140.1760.195−1.3620.3870.018
Pelteobagrus fulvidraco0.02332.880.9720.0200.0750.388−0.7160.0200.665
Cyprinus carpio0.01602.450.8310.0070.1310.2740.2990.0720.425
Acheilognathus macropterus0.02063.010.986−0.0230.1140.413−2.6820.4240.080
Hemibarbus maculates0.01103.170.9790.0440.7250.0040.1190.0210.714
Carassius carassius0.04782.830.9740.0370.5460.0010.4240.0800.272
Species PCBs
Lipid-lengthb,cCWet-lengthb,dCLipid-lengthb,e
kR2pkR2pkR2P
  • PBDE = polybrominated diphenyl ethers; PCB = polychlorinated biphenyls.

  • a

    Relationship between the body weight (w/w) and length of fish, W= A × LB, where W is body weight, L is total length, A indicates the body weight of a given length, and B indicates the peculiarity of growth 34.

  • b

    Linear regression, k is the slope.

  • c

    Relationship between the lipid content (% w/w) and length of fish.

  • d

    Relationship between the concentrations of PBDEs and PCBs (w/w) and length of fish.

  • e

    Relationship between the lipid-normalized concentrations of PBDEs and PCBs and length of fish.

Coilia ectenes taihuensis0.4500.862<0.0010.0520.3210.009−4.0100.648<0.001
Cultrichthys erythropterus0.0960.6090.0010.0220.2580.064−5.0720.784<0.001
Pelteobagrus fulvidraco0.1290.2540.094−0.0390.0970.326−5.5930.2840.075
Cyprinus carpio0.0210.0570.481−0.0020.0070.805−0.6330.1100.319
Acheilognathus macropterus0.1630.5230.043−0.1110.3850.101−11.1100.6210.020
Hemibarbus maculates0.2590.6940.0050.0410.3210.111−1.7230.1300.340
Carassius Carassius0.1580.4090.0060.0400.4910.002−1.9970.1870.0830

In most cases, positive correlations between wet weight–based concentrations of PBDEs and PCBs and fish lengths are observed (Table 3), although they are not statistically significant. A number of factors can lead to the results. Generally, a larger (i.e., longer) fish of a given species is usually older, thus being exposed to contaminants for a longer period compared with a smaller fish, which is usually younger. Therefore, this results in more PBDEs and PCBs accumulating in larger fish than in small fish. Moreover, larger fish tend to eat more of the larger prey, which may be more polluted than smaller ones. In addition, as one of the elimination pathways, increased body sizes can lead to less efficient HOC clearance over the gills, because of the reduced ratios of gill area to body volume or increased distances between HOC storage tissues and sites of elimination in the organisms 35.

However, most of the lipid-based concentrations of PBDEs and PCBs are found to negatively correlate with fish length (Table 3), especially for PCBs, although some of the correlations are not statistically significant. This phenomenon, called fish size dilution, was also reported in literature 18. It may be attributed to the different lipid contents in fish. Larger fish store more lipid than smaller ones, as supported by the positive correlations between fish length and lipid content (Table 3). As a result, the slightly higher wet weight–based concentrations of PBDEs and PCBs in larger fish were diluted by the increased lipid contents, and thus a fish size dilution effect was observed. However, it needs to be noted that fish size dilution does not mean a decrease in biomagnification of PBDEs and PCBs. It depends on the trophic position of the fish species. If a fish species is at a lower trophic position, the dilution will increase the slope of the fitted line between the PBDE and PCB concentrations and the trophic levels, indicating increased biomagnification, and vice versa. Fry were released and adult fish were caught every year in Taihu Lake. As a result, the ages of most fish in the lake usually were only one to two years. Therefore, the average concentrations of contaminants in fish of different sizes (small, medium, and large in a given species) may be better used to decrease the deviation caused by fish size dilution in investigation of biomagnification of HOCs in Taihu Lake's food chain.

Effect of logKOW and molecular size on biomagnification

The TMFs of PBDEs and PCBs increase with the increasing of logKOW, but decrease when logKOW exceeded approximately 7 (Fig. 2A), leading to parabolic relationships in which the largest TMFs are observed at logKOW of 6.89 (p < 0.001) for PCBs and 7.16 (p = 0.171) for PBDEs. Lower correlations between TMFs and logKOW for PBDEs compared to PCBs may be because of the limited data and the biodilution of some PBDEs, such as BDE138, BDE183, and BDE209, through food chains because of their biotransformation. When the combined TMFs of PBDEs and PCBs are plotted against logKOW, the largest TMFs are observed at logKOW of 7.16 (p = 0.021). Similar parabolic relationships and the highest TMFs of approximately 7 have also been reported in marine and freshwater food chains 4, 6, 8, 16, 24, 36–38. The general mechanism of biomagnification of HOCs in food chains is based on their digestion and absorption in the gastrointestinal tract 12. According to the mechanism, when the features of organisms (e.g., metabolic capacity, length, and sex) and the chemical biotransformation are not considered, the larger the logKOW values of the chemicals are, the greater their biomagnification potentials. Apparently, the biomagnification potentials of HOCs cannot be explained only by using their logKOW values. Other factors, such as the molecular sizes of the chemicals, probably play a role.

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Figure 2. Relationships between the trophic magnification factors (TMFs) and physical properties (i.e., logKOW, molecular weight and volume) of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs). The filled and open spots represent PCBs and PBDE congeners, respectively.

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The relationships between the TMFs and molecular sizes (molecular weight, volume, and diameter) of PBDEs and PCBs are assessed. Similar to those of logKOW, parabolic correlations are also observed between the TMFs and molecular weight as well as molecular volume (Fig. 2B, C). A similar relationship is also present between the TMFs and molecular diameters of PCBs (R2 = 0.261, p = 0.013), but not for PBDEs (R2 = 0.009, p = 0.957). According to the parabolic equations between the TMFs and molecular weights, the largest TMFs are observed at the molecular weights of 371 g/mol for PCBs and 563 g/mol for PBDEs, which are similar to the observations that the PCB and PBDE congeners with molecular weights of approximately 400 and 500 to 600 g/mol had the maximal bioconcentration factor through lower-trophic-level coastal marine food web, respectively 38. When plotted using molecular volumes, the largest TMFs are observed at 7.83 × 10−5 and 8.31 × 10−5 nm3 for PCB and PBDE congeners, respectively. Similarly, when the combined TMF data of PBDEs and PCBs are plotted against molecular volumes, the congener at 8.13 × 10−5 nm3 has the maximal biomagnification potential (p < 0.001). The results indicate that both PCB and PBDE congeners with the molecular volume of approximately 8 × 10−5 nm3 have the maximal biomagnification potentials.

Two main routes of HOC uptake into fish are through the gills and intestinal tract, and the two main corresponding elimination routes are via the gills and excreta 39, 40. Small molecules penetrate cell membranes more easily than large ones, which results in easier uptake as well as elimination, because passive diffusion controls the absorption of HOCs 41. However, the membrane-penetrating capability of an HOC molecule will decrease with increased size, and a molecule penetrating membranes when the maximal molecular diameter is larger than 1.5 nm is difficult 17. For the same reason, once a large molecule is absorbed by an organism, it will be difficult to eliminate it through membranes. Furthermore, higher halogenated congeners (usually the larger molecules) preferentially bind to serum proteins, which further inhibits elimination of the chemicals from the organisms 9, 42. However, biotransformation may increase the elimination rate of large molecules, which are usually highly halogenated congeners. Thus, theoretically, we should observe a peak if plotting the TMFs against the molecular volumes of the chemicals. Indeed, the present data are consistent with this speculation. The effect of the molecular volume on the HOC uptake is also supported by the observation that lowly chlorinated PCBs can be more easily absorbed via gills than highly chlorinated PCBs 39.

However, passive diffusion controls the transportation of HOCs across epithelia in an organism as previously mentioned. The transportation involves crossing an aqueous stagnant layer. Higher logKOW will decrease the solubility of the chemical, and thus lead to lower transportation, whereas biomagnification of HOCs shows parabolic correlations between the biomagnification potentials and logKOW. The present results indicate two different aspects to analyzing influences of logKOW and molecular volume on biomagnification, although similar results (the molecular volume of approximately 8 × 10−5 nm3 actually results in logKOW of approximately 7 in the present study) are observed when analyzed by using the logKOW and the molecular volumes of HOCs. However, more biomagnification investigations in which logKOW and molecular volume of an HOC are treated as more important factors are needed.

In the present study, when the combined TMFs of PBDEs and PCBs are plotted against the molecular weights, the congener with a molecular weight of 469 g/mol (p < 0.001) has the maximal biomagnification potential, which is different from the values (371 and 563 g/mol for PCBs and PBDEs, respectively) obtained when considering PBDEs and PCBs separately. Molecular volume of an HOC is usually associated with its molecular structure and molecular weight. A molecule with larger molecular weight generally has greater molecular volume if they have a similar molecular structure. However, for PBDEs, a molecule with larger molecular weight has only a slightly greater molecular volume because of the presence of a heavy bromine atom, which is supported by the slope of 1 (R2 = 0.99) for PCBs, and 0.6 (R2= 0.97) for PBDEs, by plotting their molecular volumes against their molecular weights. As a result, the difference in molecular weight between PCB and PBDE congeners leading to maximal TMFs is large (469 and 371 vs 563 g/mol), but that in molecular volume is very small (8.13 × 10−5 and 7.83 × 10−5 vs 8.31 × 10−5 nm3), no matter which TMFs of PBDEs and PCBs are used in a combined or separate way to analyze the influence of molecular size on biomagnification. Therefore, molecular volume seems better to analyze the influence of molecular size on biomagnification of PBDEs and PCBs than molecular weight, because it may reflect the essence of the processes of the uptake and elimination in biota, although several studies have used molecular weight to assess their influence on biomagnification of PBDEs 4, 17, 38.

CONCLUSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

This is the first study to report the PBDE levels and biomagnification of PBDEs and PCBs in fish from Taihu Lake, China. The PBDE and PCB contamination in fish is not significant compared with those in wild fish from other freshwater systems in China. Biomagnification occurred for most of PCBs and some PBDEs. Fish size may influence the biomagnification evaluation because of the presence of fish size dilution. Molecular size and KOW of PBDEs and PCBs can influence biomagnification of the pollutants. Parabolic correlations are observed between the TMFs and logKOW, and also between the TMFs and molecular volume. For analysis of the influence of molecular sizes of HOCs on their biomagnification potentials, molecular volumes appears to be a better metric than molecular weight.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

This research received financial support from the National Basic Research Program of China (No. 2008CB418205), the National Nature Science Foundation of China (No. 20807026), and Shanghai Leading Academic Disciplines (No. S30109).

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  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information
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Supporting Information

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. CONCLUSION
  7. SUPPLEMENTAL DATA
  8. Acknowledgements
  9. REFERENCES
  10. Supporting Information

Additional Supporting Information may be found in the online version of this article.

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