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(ProQuest: Abstract omitted; see image)[PUBLICATION ABSTRACT]
Ecotoxicology (2010) 19:623634 DOI 10.1007/s10646-009-0431-1
Bioaccumulation and biomagnication of polybrominated diphenyl ethers in a food web of Lake Michigan
Yin-Ming Kuo Maria S. Seplveda
Inez Hua Hugo G. Ochoa-Acua
Trent M. Sutton
Accepted: 9 October 2009 / Published online: 1 November 2009 Springer Science+Business Media, LLC 2009
Abstract Polybrominated diphenyl ethers are hydrophobic chemicals and can biomagnify in food chains. Little is known about the biomagnication of PBDEs in the Lake Michigan food web. Plankton, Diporeia, lake whitesh, lake trout, and Chinook salmon were collected from Lake Michigan in 2006 between April and August. Fish liver and muscle and whole invertebrates were analyzed for six PBDEs (BDE-47, 99, 100, 153, 154, and 209). Carbon and nitrogen stable isotope ratios (d13C and d15N) were also quantied in order to establish the trophic structure of the
food web. Geometric means of P PBDE concentrations in sh ranged from 0.562 to 1.61 lg/g-lipid. BDE-209 concentrations ranged from 0.184 to 1.23 lg/g-lipid in all three sh species. P BDE-47 , 99, and 209 comprised 8094% of PPBDE molar concentration. Within each sh species, there were no signicant differences in PBDE concentrations between liver and muscle. The highest concentration of BDE-209 (144 lg/g-lipid) was detected in Diporeia.
Based on analysis of d15N and PBDE concentrations, BDE-47 and 100 were found to biomagnify, whereas BDE-209 did not. A signicant negative correlation between BDE-209 and trophic level was found in this food web. Biomagnication factors were also calculated and again BDE-47 and 100 biomagnied between food web members whereas BDE-209 did not. Diporeia could be one of the main dietary sources of BDE-209 for sh in Lake Michigan; BDE-47 and 100 biomagnied within this food chain; the concentration of BDE-209 decreased at higher trophic levels, suggesting partial uptake and/or biotrans-formation of BDE-209 in the Lake Michigan food web.
Keywords Polybrominated diphenyl ethers
Decabromodiphenyl ether Biomagnication
Bioaccumulation Food web Lake Michigan
Introduction
In the 1970s, polybrominated diphenyl ethers (PBDEs) began to be commercially produced as ame retardants (Gouin et al. 2005). Because of low cost and high compatibility with plastics and fabrics, PBDEs have been applied in a variety of industrial and consumer products. For instance, PBDEs were the second most widely applied brominated ame retardants (256,660 metric tons) in the
Electronic supplementary material The online version of this article (doi:http://dx.doi.org/10.1007/s10646-009-0431-1
Web End =10.1007/s10646-009-0431-1 ) contains supplementary material, which is available to authorized users.
Y.-M. Kuo M. S. Seplveda I. Hua H. G. Ochoa-Acua
School of Civil Engineering, Purdue University, 550 Stadium Mall Dr., West Lafayette, IN 47907, USA
Present Address:Y.-M. KuoDepartment of Civil and Environmental Engineering, University of Vermont, 33 Colchester Ave., Burlington, VT 05405, USA
M. S. SeplvedaDepartment of Forestry and Natural Resources, Purdue University, 195 Marsteller St., West Lafayette, IN 47907, USA
I. Hua (&)
Division of Environmental and Ecological Engineering, Purdue University, 500 Central Dr., West Lafayette, IN 47907, USA e-mail: [email protected]
H. G. Ochoa-AcuaDepartment of Comparative Pathobiology, Purdue University, 725 Harrison St., West Lafayette, IN 47907, USA
T. M. SuttonSchool of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 245 ONeill Building, Fairbanks, AK 99775, USA
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624 Y.-M. Kuo et al.
global market between 1999 and 2003 (Bromine Science and Environmental Forum, 2006). From the Toxics Release Inventory data from 1988 to 2006, the cumulative total emissions of BDE-209 in the United States (US) were estimated to be 22,512,747 pounds (*10,212 metric tons)
from manufacturing activities (US EPA 2008).
Environmental concerns are increasing because of the ubiquitous presence of PBDEs (Hale et al. 2003). In addition, the more brominated PBDE congeners have higher octanol-water partition coefcients (Kow), and thus
are more hydrophobic (Alcock et al. 1999). Hydrophobicity is an important predictor of bioaccumulation and biomagnication. Bioaccumulation is dened as the increase of hydrophobic substances in an organism due to ingestion of contaminated food. Biomagnication refers to an increase in the concentration of hydrophobic substances in organisms at higher trophic levels. Studies with polychlorinated biphenyl (PCB) congeners indicate that the larger the value of log Kow, the higher the biomagnication potential (Fisk et al. 2001; Burreau et al. 2004). However, molecular size could be another factor affecting bioaccumulation and biomagnifation. For example, absorption of more brominated congeners (e.g., BDE-209) may be hindered in biota due to the larger molecular size ([9.5)
(Opperhulzen et al. 1985). Nevertheless, bioaccumulation of BDE-209, a fully brominated congener, has been reported in aquatic organisms; for example, levels of BDE-209 have ranged from 0.05 ng/g-lipid in polar cod (Bore-ogadus saida) to 21.6 lg/g-lipid in craysh (Cambarus puncticambarus) (Sormo et al. 2006; La Guardia et al. 2007). The P PBDEs concentrations in sh from North America were *10 times higher than Europe (Hites 2004).
The concentrations of PBDEs in sh from the Laurentian Great Lakes exponentially increased from 1979 to 2005, and sh from Lake Michigan exhibited the highest concentrations (Zhu and Hites 2004; Batterman et al. 2007). To our knowledge, there is no available data on BDE-209 concentrations in sh from Lake Michigan.
Due to a higher bioavailability and a slower elimination rate, there is increased concern about the toxicity of the less brominated congeners (Burreau et al. 1997; McDonald 2002). For example, in rodents the commercial deca-BDE mixture exhibits a much lower potential for thyroid hormone disruption compared to penta- and octa-BDE (Carlson, 1980; Zhou et al. 2001). Because of these concerns, the European Union banned the use of commercial pentaand octa-BDEs, and US manufacturers voluntarily stopped the production of these two technical mixtures in 2004 (Manugian 2004). The only PBDE mixture currently used in the US is the technical deca-BDE product. Although the no-observed-effect level (NOEL) or lowest-observed-adverse-effect level (LOAEL) of deca-BDE is considerably higher than that of BDE-47, BDE-99, or a commercial
penta-BDE mixture (Darnerud et al. 2001), neurobehavioral and carcinogenic effects after administering deca-BDE have been observed (McDonald 2002). Currently, the states of Washington (Chapter 70.76 RCWPBDEs) and Maine (LD 1658: An Act to Protect Pregnant Women and Children from Toxic Chemicals Released into the Home) legislated bans of certain uses for deca-BDE in 2007.
Lake Michigan is the largest lake within the US and the fth largest lake in the world in terms of surface area. This important freshwater resource provides great economical and ecological value. However, heavy industrialization and high population around the lake have polluted its sediments, especially in the southern region. For example, Song et al. (2005) reported that BDE-209 in sediments from southern Lake Michigan was 82.0 ng/cm2, much higher when compared to sediments from two northern sites of Lake Michigan.
The main objective of this study was to quantify bio-accumulation and biomagnication of PBDEs in a Lake Michigan food chain. We did this by quantifying concentrations of six PBDEs in plankton, Diporeia spp., Chinook salmon (Oncorhynchus tshawytscha), lake trout (Salvelinus namaycush), and lake whitesh (Coregonus clupeaformis). The present study focused on the differences in PBDE concentrations across species and tissue types (liver versus muscle). Within each sh species we also examined the correlation between PBDE concentrations and total length as well as body weight. The tropic position of each organism was determined by stable isotope analysis. To our knowledge, this constitutes the rst study on bioaccumulation and biomagnication of PBDEs in the Lake Michigan food web.
Materials and methods
Chemicals
All organic solvents were reagent grade and used as received from either Mallinckrodt (Phillipsburg, NJ) or Sigma-Aldrich (St. Louis, MO). Aqueous solutions were prepared with water puried by reverse osmosis and a Barnstead Nanopurer system (Dubuque, IA). PBDE standards were purchased from Cambridge Isotope Laboratories (Andover, MS) and Wellington Laboratories (Guelph, ON, Canada). The seven PBDE congeners analyzed in the present study were: BDE-47 (2,20,4,40-tetrabromodiphenyl ether), BDE-99 (2,20,4,40,5-pentabromodiphenyl ether), BDE-100 (2,20, 4,40,6-pentabro-modiphenyl ether), BDE-153 (2,20,4,40, 5,50-hexabromodiphenyl ether), BDE-154 (2,20, 4,40,50,6-hexabromodiphenyl ether), BDE-205 (2,3,30,4,40,5,50,6-octabromodiphenyl ether), and BDE-209 (Decabromodiphenyl ether), and BDE-205 was used as recovery standard. All
123
Bioaccumulation and biomagnication of PBDEs in Lake Michigan 625
glassware was amber and baked for 6 h at 490C to prevent contamination. No plastic supplies were used with the exception of Teon-lined caps. Teon-lined caps were solvent rinsed three times with a sequence of acidic methanol (2% HCl), methanol, and dichloromethane before use.
Biota collection
Fish and invertebrates were sampled from various locations in Lake Michigan (Fig. 1). The detailed information of aquatic organisms is shown in Tables 1S and 2S in supplemental materials. Chinook salmon (CHS, n = 6), lake trout (LAT, n = 6), and lake whitesh (LWF, n = 7) were collected in 2006 between April and June. After recording total length and weight of each individual sh, liver and dorsal muscle llets (CHS: with skin; LAT and LWF: skin removed) were dissected and separately wrapped in aluminum foil. Each tissue sample from individual sampled sh was frozen at -20C until isotope analysis and PBDE analysis. Net plankton samples (n = 4) included a mixture of phytoplankton and zooplankton; these samples were separated into four size classes using different mesh size sieves, which were #25, 35, 45, and 60. The mesh openings represent 0.707, 0.500, 0.354, and 0.250 mm openings, respectively. In addition, a sample of Diporeia spp. was collected from one location (site 6 in Fig. 1). The samples of invertebrates were collected in August 2006.
PBDE analysis
The protocol for PBDE analysis was a modied version of the US EPA method 1614 (US EPA 2007). Fish liver and
muscle, plankton, and Diporeia samples were separately homogenized using an Omni tissue homogenizer (TH-01, Marietta, GA). A subsample (at least 50 mg wet weight for each) of each homogenate was set aside for carbon and nitrogen isotope analysis. Each homogenized sample (*1 or *0.25 g for some small invertebrates) was placed in a 50-mL centrifuge tube for further lipid extraction. The samples of plankton and Diporeia were lyophilized before lipid extraction. Wet weight and dry weight were measured to the nearest 0.0001 g.
Samples were spiked with 5 ng of recovery standard (BDE-205) before lipid extraction. Total lipid content was determined via a gravimetric method (Li and Watkins 2002). Lipids were extracted by adding 21 mL of 2:1 (v/v) chloroform/methanol to each tube and then shaking for 10 min. The homogenate was then ltered through What-man (Florham Park, NJ) #40 lter paper and the original tube was rinsed with an additional 12 mL of 2:1 (v/v) chloroform/methanol. The ltered and rinsed solvents were both collected into another clean tube, and then a total of 8 mL of KCl (0.88%, w/v) was added. The mixed solution was vigorously shaken for 10 min. After mixing completely, each tube was centrifuged for 5 min at 1,000 g at room temperature and then the chloroform layer was collected for lipid determination. The solvent was evaporated by a gentle N2 stream and the dried residue was considered as the lipid of the sample.
A 10-mL aliquot of hexane was added to dissolve each crude extract. Lipid was removed by adding *4 mL of concentrated H2SO4 and the mixture was shaken for 10 min. After centrifugation (20 min, at 2,000 g at room temperature), the hexane was recovered and combined with an additional 5-mL aliquot of hexane used to wash the residue in the sulfuric acid layer. After reduction of the volume to *5 mL by a gentle N2 stream, the sample was loaded onto a glass pre-clean column (297 mm 9 14 mmi.d.) followed by 15-mL hexane. The pre-clean column was packed with 1 g sodium sulfate (Na2SO4), 3% deactivated
Florisil (8 g, 60100 mesh size, Fisher Scientic, Pittsburgh, PA), and 1.5 g Na2SO4. This eluent was collected as the rst portion of eluent. Sequentially 25 mL hexane was added onto the top of pre-clean column. The eluent was collected as the second portion of eluent. The rst portion of eluent was collected only for BDE-209 analysis and the portion of the following 25-mL eluent contained all of the PBDEs. BDE-209 concentration was based on the combination of the analyses of two portions of eluents; however, the rest of PBDEs were only eluted in the second portion. A gentle N2 stream was used to reduce the nal volume of collected eluent to 100 lL.
Samples were analyzed in a Varian 3800 gas chromatography (GC) equipped with an electron capture detector (ECD), a split/splitless injector (290C), and a VF-5ht
Fig. 1 Map of Lake Michigan indicating the locations of sampling stations
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626 Y.-M. Kuo et al.
capillary column (Varian; length 30 m, i.d. 0.25 mm, lm thickness 0.1 lm). The carrier gas was He and the makeup gas was N2. The ow rate of carrier gas was maintained at 2.2 mL/min. The oven temperature was programmed from 110C (held for 2 min) to 180C at a rate of 8C/min, to 210C at a rate of 1C/min, and to 300C at a rate of1.8C/min (held for 20 min). The concentration of BDE-209 was determined based on the analyses of the rst and second solvent elution, whereas concentrations of all other PBDE congeners were based on the analysis of the second elution only. A Thermo Finnegan Polaris Q GC equipped with an ion-trap mass spectrometry (MS) was used to ensure the identication of congeners. Electron impact ionization was utilized to ionize congeners in the MS and the GC conditions were identical to those of GC-ECD system.
Quality assurance and quality control
A solvent blank was introduced into each sample batch of GC analyses to monitor for any interference during instrumental analyses. Vegetable oil was used to simulate tissue samples and conrm the absence of interference during all analytical procedures. The method detection limit (MDL) was calculated as 3.14 times the standard deviation of each analyte in seven replicates of the method blanks (Clesceri et al. 1998). The MDL ranged from4.20 ng/g-lipid (BDE-153) to 51.3 ng/g-lipid (BDE-209). Table 3S (in the supplemental information section) shows the MDL for each congener analyzed in this study. The recovery of BDE-205 was 73 13% throughout all sample analyses. Concentrations of PBDEs were not corrected for the recovery of BDE-205. From the US EPA Method 1614, the ongoing precision and recovery (OPR) for tri- to hepa-BDEs was 50150%. Thus, the recovery percentage of BDE-205 fullls the QC acceptance criteria of US EPA Method 1614.
A coefcient of variation (CV) was selected to discriminate the large deviation of the replicates. Based on the QC acceptance criteria of US EPA Method 1614, the OPR through tri- to hepa-BDEs should range between 50 and 150% and for BDE-209 should range from 40 to 200%. Thus, when the CV of tetra- to hepa-BDEs was larger than0.5 and the CV of deca-BDE was larger than 1, the data were marked removed and not included in the statistical analysis. Using these criteria, only three BDE-209 concentrations from sh liver samples were excluded from the data set.
Stable isotope (d13C and d15N) analysis
The samples reserved for stable isotope ratio analysis were shipped to the Cornell Isotope Laboratory (Ithaca, NY) to determine stable isotope ratios for carbon and nitrogen. All
samples were freeze dried at -40C for at least 72 h and then pulverized. Subsamples (*1 mg) were weighed and analyzed by a Carlo Erba NC 2500 element analyzer coupled with Thermo Finnigan Delta Plus isotope ratio MS. Samples were standardized against Vienna Pee Dee Belemnite and air for d13C and d15N analysis, respectively.
The corresponding ratio (R) is 13C/12C or 15N/14N measured from samples and standards and d13C or d15N were calculated according to Eq. 1.
d13C or d15N& R
sample=Rstandard 1 1000
1
To ensure the precision of the instrument, Cayuga Brown Trout (CBT, an in-house standard) was provided by the International Atomic Energy Association and calibrated on a biannual basis. CBT was analyzed after every eight samples. For this analytical run the overall standard deviation of CBT was 0.06% for d15N and 0.05% for
d13C. The accuracy of the instrument was examined across the sample levels by using a chemical methionine standard.
The trophic level of organisms is expressed by this continuous parameter (d15N) instead of traditional classications because it is implausible that an organism feeds from only one trophic level. By using Eq. 2 to combine the information about trophic structure and PBDE concentrations in the food web, the biomagnication of PBDEs through trophic transfer can be determined (Broman et al. 1992; Rolff et al. 1993).
c A eB d
15N
2
In Eq. 2, c is the concentration of individual PBDE congeners in organisms in which the value of d15N is also
analyzed. A is a constant which does not change with trophic level. B indicates the biomagnication potential of individual PBDE congeners: a positive B value means that PBDE concentration is magnied at the higher trophic level(i.e., biomagnication). In contrast, a negative B value means PBDE concentration decreases with increasing trophic level, which implies that biotransformation and/or partial uptake might have occurred at higher trophic levels. For each specic predator and prey relationship, the biomagnication factor (BMF) was calculated using Eq. 3.
BMF PBDE
predator
=PBDEprey 3
Data analysis
An analysis of variance (ANOVA) followed by a Tukeys multiple comparison test was used to determine differences in PBDE concentrations among different sh species and tissues (SAS Institute, Inc., Cary, NC). Linear regression models were used to interpret the relationships between PBDE concentrations and lipid content, total length of sh,
123
Bioaccumulation and biomagnication of PBDEs in Lake Michigan 627
body weight of sh, and trophic levels. For the purposes of statistical analysis, any concentration below the detection limit was assigned the value of one-half of the MDL to calculate the geometric mean of replicates (Nehls and Akland 1973). Tissue concentrations were log-transformed prior to statistical analyses to meet the assumption of normality. Signicance differences were declared when P \ 0.05.
Results and discussion
PBDE concentrations in biota
Mean concentrations of individual PBDE congeners in sh and invertebrates are shown in Fig. 2. With the exception of BDE-209, the lowest concentrations of PBDEs were measured in plankton with most PBDE congeners being below the MDL. The lowest concentration of BDE-209(0.184 lg/g-lipid) was found in LAT liver. Only one
Diporeia sample was available during 2006 for PBDE analysis. The concentration of BDE-209 in Diporeia was relatively high (144 lg/g-lipid). To further validate this data, an additional Diporeia sample was collected from Lake Michigan in June 2008 (site 8 in Fig. 1). BDE-209 concentration measured from this sample was still quite high (234 lg/g-lipid). Diporeia are benthic organisms living in close proximity to sediments (Fraser et al. 2005). Higher concentrations of BDE-209 compared to other congeners have been reported for sediments from Lake Michigan. Song et al. (2005) quantied PBDEs in sediments from Lake Michigan and found that the concentrations of BDE-209 were at least one order of magnitude higher than the sum of the other nine common PBDEs (on a mass basis). Similar results have been reported for sediments downstream from wastewater efuents (La Guardia et al. 2007; Labandeira et al. 2007). Thus, sediments are a likely source of BDE-209 to Diporeia in Lake Michigan.
In zooplankton, PBDE concentrations did not vary much by plankton size (Fig. 2); however, the smallest plankton
Fig. 2 Individual PBDE concentrations (mean SE) in different organisms from Lake Michigan. Note that PBDE concentrations are plotted using different scales. BDE-47 and 100 increased with trophic level. ND not detected
0.35
0.18
BDE-99
BDE-47
0.3
0.15
0.25
0.12
0.2
0.09
0.15
0.06
0.1
0.05
0.03
ND
ND
0
0
0.09
0.04
PBDE conc. ( g/g-lipid)
0.08
BDE-100
BDE-153
0.07
0.03
0.06
0.05
0.02
0.04
0.03
0.02
0.01
0.01
ND
ND
ND
ND
ND
ND
0
0
0.04
160
BDE-154
BDE-209
140
0.03
120
100
0.02
80
60
0.01
40
ND
ND
ND
20
0.84
1.50 1.23 0.18
0.26
0.65 0.73
0
0
Plankton-60
Plankton-45
Plankton-35
Plankton-25
Diporeia
LWF-liver
LWF-muscle
LAT-liver
LAT-muscle
CHS-liver
CHS-muscle
Plankton-60
Plankton-45
Plankton-35
Plankton-25
Diporeia
LWF-liver
LWF-muscle
LAT-liver
LAT-muscle
CHS-liver
CHS-muscle
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628 Y.-M. Kuo et al.
(i.e., plankton-60) had higher PBDE concentrations. This phenomenon is likely due to the attachment of detritus (i.e., organic particles) and thus PBDEs on plankton. There is evidence showing that not only suspended solids but also microorganisms can sorb hydrophobic substances (PCBs-Aroclor 1254), and live algae are capable of an increased PCB sorption rate compared to dead (Weber et al. 1983). In addition, smaller plankton have higher specic surface areas for more PBDE sorption. Thus, sorption might play an important role in the differences of PBDE concentrations observed in plankton.
The total PBDE concentration for each tissue was calculated as the summation of six congeners: BDE-47, 99, 100, 153, 154, and 209. The PBDE concentrations (on a lipid weight basis) of each congener in the liver and muscle of CHS, LAT, and LWF are shown in Fig. 2. Highest concentrations of BDE-47 (0.588 lg/g-lipid), BDE-99(0.298 lg/g-lipid), and BDE-209 (4.64 lg/g-lipid) were detected in a sample of LWF muscle. The highest mean concentration of P PBDE , 1.61 lg/g-lipid, was also found in a sample of LWF muscle. There were no statistically signicant differences between liver and muscle PBDE concentrations within each sh species. This is in accordance with the report by Vives et al. (2004), and suggests a uniform distribution of BDE-47, 99, 100, 153, 154 between liver and muscle in the sh studied.
The molar proportions of PBDEs were distinct for each sh species studied (Fig. 3). For both liver and muscle, the predominant congeners were BDE-209, 47, and 99.
BDE-209 accounted for *50, *25, and *60% of the PBDEs in CHS, LAT, and LWF, respectively. BDE-209 concentrations in both liver and muscle of CHS (0.490 and0.727 lg/g-lipid) and LWF (0.754 and 1.23 lg/g-lipid) were signicantly higher than LAT (0.184 and 0.259 lg/g-lipid). Higher accumulation of BDE-209 in LWF might be due to Diporeia consumption (Pothoven 2005). On the other hand, BDE-47 accounted for *50% of the P PBDEs in LAT.
Across all sh tissues and invertebrates, individual PBDE concentrations (on a wet weight basis) were signicantly and positively related to lipid content except for BDE-209, for which no signicant trends were observed (Fig. 4). The reason behind this lack of relationship with lipid content is likely due to the fact that BDE-209 has a higher afnity with serum proteins instead of lipids (Morck et al. 2003). In contrast, the positive linear trends observed for BDE-47, 99, 100, 153, and 154 suggest bioaccumulation of PBDEs is correlated with lipid content since higher lipid content increased the capacity for PBDE accumulation. Livers from LAT had the highest lipid content (23%) and the highest BDE-47, 99, 100, 153, and 154 concentrations (68.0, 18.6, 20.9, 8.37, and 10.3 ng/g on wet weight basis, respectively). These results also suggest biomagnication is taking place in this food chain since invertebrates had much lower BDE-47 concentrations than sh tissues. However, this trend was not apparent as the degree of bromination increased.
PBDE concentrations and total length/body weight of sh
To further examine bioaccumulation in sh, the relationships between PBDE tissue concentrations and total length as well as body weight were evaluated. From previous research, PBDE levels increased with sh size (Hale et al. 2001; Eljarrat et al. 2004); however, Rice et al. (2002) reported no correlation between PBDEs and length or weight in common carp (Cyprinus carpio) collected from the Detroit River. Labandeira et al. (2007) found that these two relationships existed in wild carp at different sites. In our study, inconsistent relationships were also observed. There was no signicant relationship between PBDEs and total length or body weight in tissues of either CHS or LWF; however, BDE-47, 99, 100, 153, and 154 concentrations in liver and muscle increased with total length and body weight in LAT (see Figs. 1S and 2S of supplemental information). These results may be explained by the likelihood that larger (possibly older) LAT were exposed to PBDEs for a longer period of time compared to smaller (possibly younger) sh. In addition, larger sh may eat larger or more polluted prey. The regression coefcient (r2)
of individual PBDE congeners was larger when total length was the explanatory variable compared to body weight.
BDE-209 BDE-154 BDE-153 BDE-100 BDE-99 BDE-47
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
CHS-liver
CHS-muscle
LAT-liver
LAT-muscle
LWF-liver
LWF-muscle
Fig. 3 Molar proportion of PBDE congeners in liver and muscle of sh (CHS Chinook salmon, LAT lake trout, LWF lake whitesh). The molar proportions differ across species. Data are the average of six or seven samples
123
Bioaccumulation and biomagnication of PBDEs in Lake Michigan 629
9
Fig. 4 Plots of lipid content vs. individual PBDE concentrations (ng/g-wet wt). With the exception of BDE-209, signicant positive linear trends were observed for all PBDEs, suggesting bioaccumulation related to lipid
9
BDE-47
BDE-99
y = 0.121 x + 0.766 r2 = 0.284
7
7
y = 0.095 x + 0.136 r2 = 0.371
5
5
3
3
1
1
-1
-1
-3
0 5 10 15 20 25
-3 0 5 10 15 20 25
9
9
ln PBDE conc. (ng/g-wet wt.)
BDE-100
7
BDE-153
7
y = 0.148 x - 0.499 r 2 = 0.406
y = 0.153 x - 1.511 r2 = 0.560
5
5
3
3
1
1
-1
-1
-3
-3 0 5 10 15 20 25
0 5 10 15 20 25
9
9
BDE-154
BDE-209
7
7
y = 0.150 x - 1.300
r2 = 0.541
5
5
3
3
1
1
-1
-3
-1
-5 0 5 10 15 20 25
-3 0 5 10 15 20 25
Lipid %
Invertebrate Fish liver Fish muscle
Fish species comparison
From previous PBDE studies of sh from the Laurentian Great Lakes, lake trout and rainbow smelt (Osmerus mordax) from Lake Michigan were found to contain the highest PBDE concentrations (Zhu and Hites 2004; Batterman et al. 2007). Both studies report that one exponential model could appropriately t PBDE concentrations in sh during the period of 19792000. Thus, they concluded that PBDE concentrations in sh from the Laurentian Great Lakes doubled every 24 years. Manchester-Neesvig et al. (2001) analyzed PBDEs in Coho salmon (Oncorhynchus kisutch) and Chinook salmon in 1996 and Zhu et al. (2004) detected PBDEs in lake trout from Lake Michigan in 1996 and 1997. All of these studies reporting P PBDEs in sh from Lake Michigan are summarized in Table 1. In the present study, the geometric mean concentrations of P PBDEs
(BDE-47, 99, 100, 153, and 154) ranged from 0.254 to0.389 lg/g-lipid, which are lower than other published reports. However, data from published articles were obtained from the analyses of the composites of whole or partial sh. Because this study did not include an analysis of PBDEs in adipose tissue, the lower concentrations may reect differences in PBDE distribution in different compartments (e.g., liver and muscle versus adipose).
A few studies have been published indicating that wild sh are able to accumulate BDE-209. Table 2 summarizes literature reports of BDE-209 concentrations in sh. BDE-209 concentrations have ranged from sub-ppb to ppm levels (2.88 lg/g-lipid of sunsh, Lepomis gibbosus).
The mean level of BDE-209 in different tissues quantied in the present study (0.1841.23 lg/g-lipid) was slightly higher than most reported data. The relatively high concentration of BDE-209 in sh tissues might indicate that
123
630 Y.-M. Kuo et al.
Year Fish species P PBDEs (lg/g-lipid) Reference
1996 Salmon 2.01 Manchester-Neesvig et al. (2001)
1996 Lake trout 1.254 Zhu and Hites (2004)
1997 Lake trout 1.030
2000 Lake trout 0.823a Batterman et al. (2007)
2004 Smelt 1.6a
2006 Chinook salmon (liver) 0.285b/0.299c This study
Chinook salmon (muscle) 0.358b/0.417c
Lake trout (liver) 0.377b/0.425c
Lake trout (muscle) 0.380b/0.450c
Lake whitesh (liver) 0.254b/0.292c
Lake whitesh (muscle) 0.389b/0.486c
Table 2 Summary of published mean concentrations of BDE-209 in free-ranging sh
Location Fish species Tissue BDE-209 concentration Reference
Inland Sea of Seto, Japan Eel, gray mullet, horse mackerel, red sea bream, sea bass, ounder
Muscle with skin Sea bass 0.40.81 ng/g-lipid Akutsu et al. (2001)
Flounder 1.93.2 ng/g-lipid
Svalbard, Norway Cod Whole sh 0.050.42 ng/g-lipid Sormo et al. (2006)
Baltic sea and northernAtlantic Ocean
Table 1 Summary of mean PPBDEs (BDE-47, 99, 100, 153, and 154) concentrations (lg/g-lipid) in sh from Lake
Michigan
a BDE-47, 99, 100, 153 only; the lipid content of lake trout and smelt was 17.5 and 5.0%, respectively
b Geometric mean
c Arithmetic mean
Sprat, herring, salmon Skinless muscle Sprat 0.082 ng/g-lipida Burreau et al. (2006)Herring 0.24 ng/g-lipida
Salmon 0.41 ng/g-lipida
Lake Winnipeg, Canada Walleye, whitesh, emerald shiner, goldeye, white sucker, burbot
Whole sh 3.6198.68 ng/g-lipid Law et al. (2006)
Vero River, Spain Carp, barbel Muscle Carp 79.5 ng/g-lipid Eljarrat et al. (2007)
Barbel 195 ng/g-lipid
Wastewater receiving stream, USA
Chub, sunsh Whole sh Sunsh 2.88 lg/g-lipid La Guardia et al. (2007)
Lake Michigan, USA Chinook salmon Liver 490b/605c ng/g-lipid This study
Chinook salmon Muscle 727b/894c ng/g-lipid
Lake trout Liver 184b/205c ng/g-lipid
Lake trout Muscle 259b/263c ng/g-lipid
Lake whitesh Liver 754b/970c ng/g-lipid
Lake whitesh Muscle 1.23b/1.54c lg/g-lipid
a Median
b Geometric mean
c Arithmetic mean
Lake Michigan could be signicantly contaminated with BDE-209.
Isotope analysis
Primary producers between pelagic and benthic realms differently assimilate 13C (Keeley and Sandquist 1992). Benthic algae are enriched in 13C compared to pelagic algae and/or particulate organic matter (POM). Thus, d13C
can be used to trace back the carbon ow of primary
producers in food webs (France 1995). The d15N also
reects the hierarchy along the food chain. An enriched level of 15N in tissues is indicative of organisms in higher trophic level (DeNiro and Epstein 1981; Minagawa and Wada 1984). The d13Cd15N plot of all the aquatic
organisms sampled in this study is shown in Fig. 5. Each sh species was divided into two groups by the median total length. The total lengths of CHS, LAT, and LWF were 405852, 539695, and 373575 mm, and the smaller groups of CHS, LAT, and LWF were 405600, 539591,
123
Bioaccumulation and biomagnication of PBDEs in Lake Michigan 631
18
-32 -30 -28 -26 -24 -22 13C
CHS-small CHS-large LAT-small LAT-large LWF-small LWF-large Diporeia Plankton-25 Plankton-35 Plankton-45 Plankton-60
16
14
12
15 N
10
8
6
4
Fig. 5 d13C and d15N ratios (mean SE) for aquatic organisms sampled from Lake Michigan
and 373529 mm, respectively. However, there was no evidence of increased stable isotope ratios in sh tissues due to different sizes. The depleted d13C (-30.9 to
-29.1%) for all the plankton samples indicates these organisms belong to a pelagic food web, whereas the sh tissues and Diporeia had enriched d13C values (-26.7 to -23.2%) indicating a more benthic habitat. LWF is a bottom feeder which primarily feeds on Diporeia, insect larvae (Chironomidae), Dreissena polymorpha, and Mysis relicta. Diporeia comprised *40% of total dry weight diets of LWF from Lake Michigan (Pothoven 2005), which explains the enriched d13C found in LWF tissues. LAT muscle had the highest d15N values, which suggest these sh were highest in the food chain. LAT and CHS are pelagic but feed in both pelagic and benthic realms (Brandt 1986; Eck and Wells 1986). Thus, enriched d13C ratios
were also found in both sh.
There are many factors that can explain variations in stable isotope ratios in invertebrates. Stable isotope ratios provide an averaged diet information over a period of time, and organisms change their feeding habits during their lifespan (Fraser et al. 2005; Pothoven 2005). This observation can likely explain why freshwater zooplankton samples have a wide range in d15N values (i.e., 317%)
(France 1994). A large variation in d15N values in zoo-plankton was also found in the present study. Although Stapleton et al. (2001) also reported large variations in d15N in zooplankton from Lake Michigan, it was due to seasonal shifts. Our zooplankton samples were collected in August 2006 only. So the variations observed might be due to having sampled plankton from different locations.
We found relatively high lipid content (4373% on a dry weight basis) in plankton samples, which were collected in August. Vanderploeg et al. (1992) also reported that the lipid content measured from adult female Diaptomus sicilis, a kind of zooplankton, reached a plateau in summer. On the other hand, differences in d13C and d15N between lipid-extracted and non-extracted samples have been investigated in previous studies, and values of d13C and d15N are higher for extracted lipid samples (Murry et al. 2006). Because our plankton samples for stable isotope analysis were not lipid-extracted, this lipid bias might also explain the large variation observed in d15N for some zooplankton samples.
PBDEs in trophic positions
Figure 2 illustrates PBDE concentrations in organisms sampled in the present study. A signicant biomagnication of BDE-47 and 100 was observed. To further quantify biomagnication relationships, the correlations between lipid normalized PBDE concentrations of aquatic organisms and their respective stable isotope ratios were investigated. In sh liver and muscle tissues as well as invertebrates, BDE-47 and 100 were found to biomagnify, whereas concentrations of BDE-209 decreased with increasing trophic levels (Table 3; Fig. 6). In the study by Burreau et al. (2004), the B values for BDE-47, 99, 100, 153, and 154 were signicantly larger than 0.5 , although the B value for BDE-209 was reported as a negative value which did not signicantly differ from zero. Our B values for BDE-47 and 100 were similar to Laws ndings (Law et al. 2006) (Table 3), although these authors did not observe signicant biomagnication for these two congeners. In contrast to our results, they reported signicant
d15N-liver d15N-muscle d15N-musclea
B P r2 B P r2 B P r2
BDE-47 0.361 0.019 0.569 0.375 0.022 0.553 0.434 0.09 0.46 BDE-99 -0.007 0.955 0.0004 0.001 0.996 0 0.107 0.78 0.02
BDE-100 0.295 0.001 0.837 0.268 0.008 0.717 0.289 0.27 0.24
BDE-153 -0.040 0.804 0.011 0.054 0.584 0.053 b
BDE-154 0.138 0.250 0.213 0.088 0.415 0.113
BDE-209 -0.645 0.023 0.452 -0.606 0.017 0.486 0.616 0.01 0.74
Table 3 Comparison of statistical parameters from PBDE biomagnication model tted with d15N
a Data from Law et al. (2006)
b Not applicable
123
632 Y.-M. Kuo et al.
7
7
Fig. 6 Stable nitrogen isotope ratio vs. BDE-47, 100, and 209 concentrations in sh liver (left column), sh muscle (right column), and invertebrates. Two compounds, BDE-47 and BDE-100, biomagnied, but BDE-209 was only partially accumulated within this food web
LAT-large
6
6
LAT-large
LWF-large
5
CHS-large
CHS-small
LWF-large
LWF-small
LAT-small
5
CHS-small
CHS-large
LAT-small
LWF-small
Diporeia
4
4
Plankton-60
3
Plankton-25
BDE-47y = 0.361 x + 0.522 r2 = 0.569; P = 0.019
BDE-47y = 0.376 x + 0.564 r2 = 0.553; P = 0.022
3
Plankton-25
Plankton-60
Diporeia
2 4 6 8 10 12 14 16 18
2 4 6 8 10 12 14 16 18
1 4 6 8 10 12 14 16 18
4 4 6 8 10 12 14 16 18
ln PBDE conc. (ng/g-lipid)
5
5
LAT-large
LAT-large
LWF-large
LWF-small
4
CHS-large
CHS-small
LWF-large
LWF-small
4
CHS-small
CHS-large
LAT-small
Diporeia
3
3
2
Plankton-60
2
Plankton-60
Diporeia LAT-small
BDE-100y = 0.295 x + 0.369 r2= 0.837; P = 0.001
BDE-100y = 0.268 x + 0.638 r2 = 0.717; P = 0.008
1 4 6 8 10 12 14 16 18
4 4 6 8 10 12 14 16 18
13
13
12
Diporeia
BDE-209y = -0.645 x + 14.792 r2 = 0.452; P = 0.023
12
Diporeia
BDE-209y = -0.606 x + 14.506 r2 = 0.486; P = 0.017
11
11
10
10
Plankton-60
Plankton-60
9
Plankton-35
Plankton-45
9
Plankton-35
CHS-large
Plankton-45
8
8
Plankton-25
Plankton-25
LWF-small
7
7
CHS-small
CHS-small
LWF-large
LWF-small
LWF-large
6
CHS-large LAT-large
6
LAT-small
LAT-large
5
LAT-small
5
15N
Table 4 Lipid-adjusted biomagnication factors for individual PBDE congeners measured from sh (Chinook salmon, CHS; lake whitesh, LWF; lake trout, LAT) and Diporeia
Predator/prey Tissue BDE-47 BDE-99 BDE-100 BDE-153 BDE-154 BDE-209
LWF/Diporeia Liver 1.48 0.40 1.45 0.12 0.30 0.01
Muscle 2.25 0.73 1.52 0.33 0.37 0.01
CHS/LWF Liver 1.12 0.88 1.14 1.14 2.91 0.78
Muscle 1.07 0.61 1.09 0.82 1.13 0.59
LAT/LWF Liver 1.59 0.89 1.41 4.42 3.19 0.22
Muscle 1.17 0.49 1.18 1.43 1.44 0.21
biomagnication for BDE-209. A negative B value for BDE-209 in our study suggests either that BDE-209 was not taken up by organisms at higher positions in the food chain or that biotransformation of this congener occurred while trophic transfer within members of Lake Michigan food web. Note that due to very low PBDE concentrations in organisms from lower trophic levels, data from plankton-60 predominantly contributed to the regression analyses of BDE-47, 99, 100, 153, 154.
Lipid-normalized BMFs for each PBDE congener between individual predator and prey are presented in
Table 4. BMFs for BDE-47 and 100 are all larger than one(1.07 to 2.25 and 1.09 to 1.52, respectively). A BMF larger than one suggests biomagnication in the specic predator/ prey relationship. Thus, calculated BMFs indicate that BDE-47 and 100 biomagnify in all feeding relationships. In contrast, BMFs for BDE-209 were all less than one ranging from 0.01 to 0.78. These ndings are consistent with the results obtained using linear regression with d15N.
Biomagnication and biotransformation of PBDEs are related to the specic metabolism and dietary habit of each species. This can explain why BMFs of a PBDE congener
123
Bioaccumulation and biomagnication of PBDEs in Lake Michigan 633
differ in different trophic interactions. Law et al. (2006) reported BMFs for BDE-47 and 100 that ranged from 0.1 to8.9 and from 0.1 to 4.9, respectively, and the highest BMF was 34 for BDE-209 in a study with goldeye (Hiodon alosoides) and zooplankton. Different biomagnication potentials and BMFs are usually reported for a chemical across locations. These differences result from differences on organisms sampled in the food webs, different sampled food web lengths, and many other ecological factors (e.g., seasons). These also suggest the inherent differences between studies.
Conclusions
Bioaccumulation and biomagnication were investigated in a food web from Lake Michigan. From the PBDE analyses of sh liver and muscle, BDE-47, 99, and 209 were three predominant congeners comprising 8094% of PBDE molar concentration. Although there were no signicant differences between liver and muscle for individual PBDE congeners within each sh species, the congener distributions differed between species. Moreover, BDE-209 was quantied in all sh samples (0.184 to 1.23 lg/g-lipid).
These mean levels of BDE-209 in sh tissues are higher than previously reported data, indicating Lake Michigan is contaminated with BDE-209.
Bioaccumulation of individual PBDE congeners varied across species. For example, in LAT tissues only, concentrations of lower brominated congeners (BDE-47, 99, 100, 153, and 154) increased with total length. That might result from either longer exposure or eating larger and more contaminated prey. There are signicant positive correlations between the lipid content and the concentrations of BDE-47, 99, 100, 153, and 154 in organisms. However, bioaccumulation of BDE-209 did not increase with lipid content, suggesting BDE-209 accumulation might be controlled by protein transport during absorption.
The BMF calculation and the analysis of d15N and
PBDE concentrations indicated that BDE-47 and 100 bio-magnify. However, BDE-209 concentrations decreased at higher trophic levels, suggesting partial uptake and/or biotransformation of BDE-209 in the food web of Lake Michigan.
Acknowledgments The authors thank the Michigan Department of National Resources for helping collecting the sh and Walter Bialkowski and Kimberly Ralston-Hooper for their help with invertebrate sampling. We also thank the Cornell Isotope Laboratory for stable isotope analysis as well as Dr. Changhe Xiao, Dr. Anant Bharadwaj, and Juan Bezares-Cruz for laboratory assistance. This work was nancially supported by the US EPA Great Lakes National Program Ofce (GLNPO): Ecotoxicology of Brominated Flame Retardants in Great Lakes Biota (Project number GL2005-139). The conclusions in this article do not necessarily reect those of GLNPO.
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