Environ. Sci. Techno/. 1995, 29, 2010-2015
Uptake of PCBs in Fish in a Comtamhated River System:
GUDRUN BREMLE, LENNART OKLA, AND PER LARSSON* Ecotoxicology,Department of Ecology, Lund University, 223 62 Lund, Sweden
W e have studied PCB concentration and domain (one to three congeners) distribution in water and fish along a gradient of a contaminated river system. The river was contaminated by a small lake that contains about 400 kg of PCB in the sediment. The PCB concentration in water in the outlet from the lake was 8.6 ng/L, which was 12 times higher than upstream. PCB concentration in fish from the lake was about 20 times higher than the concentration in fish from upstream lakes. The polluted lake considerably influenced domain distribution in both water and fish. The fish bioconcentration factors (BCFs) for low to highly chlorinated domains showed a bell-shaped curve. BCFs for low chlorinated PCBs were less than for more highly chlorinated ones, but for the largest molecules the BCFs were reduced. The bell-shaped curve remained also when domain numbers were transformed into corresponding log K,,values. BCFs for the same domains were shown to vary between stations.
Introduction The river EmAn in southern Sweden is contaminated by PCBs. The main source is the sediments of Lake Jitrnsjon, which contains about 400 kg of PCB. The concentration inthesedimentvariesbetween 10.002to31pg/gdryweight. About 5.6 kglyear is transported downstream to the Baltic Sea. The sediment in the lake is mixed with fibers emanating from a paper mill. It was probably the handling of recycled paper at the mill that caused the contamination, especially PCB-containing self-copying paper from old archives ( I ) . When PCBs are dispersed into the environment, their distributionis controlledby a number of chemical,physical, and biological processes and properties, such as water solubility,lipophilicity,vapor pressure, adsorption to soils and sediments, bioconcentration in fish, biodegradation, photolysis, hydrolysis, and oxidation (2). The outcome is thus difficult to predict. Pollutants adsorb to suspended particles in the water and will sooner or later be associated with the sediment (3). However, when the concentration in the water
2010 rn ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 8,1995
decreases, the sediment can act as a source to the water (2). The ability of the sediment to keep nonionic organic compounds is positively correlated to the organic content (4-6). The organisms within the sediment also influence the migration and the partitioning of pollutants (7). The uptake of nonionic organic compounds by organisms acts as a partitioning between the water and the organism’s fat pool via the IUS (bioconcentration) and/or intake from food over the guts (8, 9). In laboratory experiments with fish, it has been shown that nonionic organic pollutants are taken up via the gills from the water. The concentrationwithin the organism rises fast to a steady state. If the concentration in the water increases,the uptake rate for the organism will be faster, and it will level off on a higher steady-state concentration (10). BCF (bioconcentration factor) is a constant describing the concentration of a chemical in the water to its concentration in an aquatic animal at equilibrium:
BCF = concentrationaquatic a,imd/concentration,,,,,,, In the hydrophobicity model (101, the partitioning of the chemical between the water and the lipid phase of the fish is controlled principally by the activity (concentration) gradient and, thus, by the diffusion. No physiological barrier is assumed to exist. Uptake and elimination exhibit first-order kinetics, i.e., BCF will be independent of the exposure concentration (10). BCF is also assumed to be directly proportional to the octanol/water partitioning coefficient (the lipophilicity of the compound, 11). The hydrophobicity model has, however, proved to be too simple,and several alternativemodels have been presented (10). Those models predict the importance ofphysiological control of the uptake, steric hindrance of large molecules, distribution of the chemical within the organism, biotransformation of the chemical, and biodegradation. In the field, the food for fish as well as the water is contaminated. There is, thus, an additive uptake via the food (11). The relative importance of the different uptake routes are disputed (12, 13). They seem to be dependent on species,exposure situation, food web, and the physicalchemical properties of the contaminant (9). The aim of this study was to examine the distribution of PCB congeners between water and fish in a gradient of a river system contaminated by a low chlorinated PCB mixture. Special interest was paid to the concept of bioconcentration. Are there variations of BCFs between different locations with different contaminant exposure? How do BCFs differ in relation to liphophilicityof the PCB congeners?
Materials and Methods Sampling. PCB in water was continuously measured at five stations during the summer and autumn of 1991at the two upstream locations, nos. 2 and 4; the contaminated Lake Jitrnsjon (no. 5); and the downstream locations, nos. 6 and 8 (Figure 1). The sampling method is described earlier (1). About 100 L of river water was pumped through polyurethane columns (PUC) at a flow rate of 10 mL/min. The PUCs were changed weekly. Both dissolved and particle-bound PCBs were collected by the columns. Fish were caught with gill nets during August 1991at four sites,
0013-936W95/0929-2010$09.00/0
0 1995 American Chemical Society
TABLE 1
Domain Correspondence to Congener (IUPAC No.) According to Schulz et a/. (15) domain IUPAC Nos. domain
0
IO
20 Km
2 BALTIC SEA
7
FIGURE 1. River Emin in southern Sweden with the different sampling stations. The size of lake JLIrnsjlln (no. 5) is exaggeratedforvisibility. Water samples were taken at station nos. 2,4,5,6, and 8. Fish was caught in nearest possible lake, station nos. 1, 3, 5, and 7.
nos. 1,3,5,and 7 as close to the PCB sampling stations as possible. Ten perch (Perca fluviatilis L., 1-year-old, 5 females and 5 males, weighing4.9- 10.0 g) were taken from each location. Fish and water samples were stored in a freezer until analyses. Sample Preparation. The PUC was freeze-dried to complete dryness. Whole fisheswere weighed, cut to pieces, and freeze-dried. The dry fish was weighed again and pulverized. A portion of about 2 g was transferred to a glass extraction vial. PCBs in the fish and in the PUC were extractedwithacetone(Merck, 12p.a. z.r.):n-hexane (Merck, 4371 p.a. z.r.),10:7v/v, in a modified Soxhlet apparatus for 2 h. Octachloronaphthalene was used as an internal standard and was added prior to the extraction. The PUC extracts were subjected to a water equilibrium to separate the acetone and polar impurities, after which the hexane fraction was evaporated in a vacuum centrifuge (Savant). The fish extracts,which contain fat,were evaporated directly in the vacuum centrifuge, and the fat content was determined gravimetrically. To clean the samples, an open column step was performed. A silica gel column was prepared by adding 4 mL of activated silica gel (Merck, 7754 60 reinst 70-230 mesh) soaked with 1 g of concentrated sulfuric acid 99% [Merck,731p.a.and721p.a. (fumic)]to 18mLoftheeluation liquid, a mixture of n-hexanedichloromethane(Merck,6054 p.a. z.r.1, 95:5 vlv, in a glass column. When this gel was sedimented, 4 mL of a silica gel soaked with 1 mL of 1 M K2CO3 (aqueous pH 11) (Merck,4928 p.a.1 was added. The basic gel withdraws acidic substances (e.g., fatty acids), and the acidic gel oxidizes and retains nonpersistent compounds. To keep the gel in place, a porous polypropylene disk was placed on top. The solvent in the packing step was eluated, and another 5 mL of eluation liquid was added to rinse the column. The evaporated samples of both water and fish were dissolved in n-hexane (includingrinsing a total volume of 1.2 mL) and transferred to the silica gel column. A total of 3 mL of eluation liquid was added, and the eluate was discarded. The eluate of the next 5 mL of eluation liquid
1 2 3 4 5 6 7 8 9 10 '1 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
10,4 7,9 6 8,5 19 18,17,15 24,27 16,32 34 29 26 25 31,28 20,33,53 51,22 45 46 69 52 49 47,48,75 35 44 37,59,42 41,64 96 40 100,67 63
30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
IUPAC Nos. domain 74 70 66,95 88 91 60,56 92 84 90,101 99 119 83 97 87.115 85 136 77,110 82, 151 135 107 123,149,118 134 114,131, 122 146 132,153, 105 141,179 130 176, 137 160,138,158
59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87
IUPAC Nos. 129,126,178 175 187 183 128 167 185 174 177 202, 171,156 173,157,201 172 197 180 193 191 200 169 170, 190 198 199 203, 196 189 208, 195 207 194 205 206 209
added was collected. This collected eluation volume that contains the PCBs was placed in a vacuum centrifuge, and the solvent was evaporated, after which 400,uL of isooctane (Merck, 4727 p.a.1 was added. Analysis. Samples were analyzed for PCBs by capillary gas chromatographylECD on a Shimadzu (GC- 14A) equipped with splitlsplittless injector. The PCB components were separated on a 20-m DB-5 quartz capillary column (i.d. 0.18 mm, Rtx-5, Restek Corp.) with Hz (1.5 mLlmin) as carrier gas and NZ(50mLlmin) as makeup gas. Oven temperature was programmed to keep the initial temperature at 80 "C for 15 min, then to rise 4 "C/min to 300 "C, and to hold it for 15 min. The injector and the detector temperatures were 310 and 320 "C, respectively. The peaks were automatically integrated (Schimadzu C-R5A) and stored on a computer. PCB components were identified and quantified according to Mullin et al. (14) and Schulz et al. (15). As a chromatographic standard (to check retention and response), pentachlorobenzene was used. The analytical performancewas regularly controlled with PCB standards as Aroclor 1242 and ClophenA60. Domains that could not be properly qualitatively or quantitatively analyzed were excluded from the analysis. Table 1 translates domain to congener (IUPAC No.) according to Schulz et al. (15). When analyzed on a capillary gas chromatograph/ECD with a DB-5 column, the resolution of the 209 PCB congeners is not complete. Some of the congeners will coelute. The peaks within the chromatogram, which are called domains, consist of one to three congeners (15).For the sake of simplicity,they can be treated as one component since in many aspects they have the same chemical properties. The relative amounts of congenerscomposing a domain though differ among sample types and commercial mixtures (15). VOL. 29,
NO. 8. 1995 / ENVIRONMENTAL SCIENCE 81 TECHNOLOGY 201 1
TABLE 2
Concentration of XPCB in Water of River Emiin at Different Stations (Geometricameans, n = 10) and the Calculated PCB Transporte water station
2 4 5 6 8
concn (ngA)
fish transport (g/day)
0.7 (0.4-1.0) 1.2 (0.9-2.4) 8.6(4.2-20.8) 5.1 (2.0-10.6) 1.3(0.7-3.3)
station
concn (ng/g wet w )
1 3 5
37.3 (20.6-63.3) 273 (192-394) 825 (513-1244)
7
221 (122-341)
0.15 (0.09-0.24) 0.59 (0.25-1.76) 4.57 (1.01-9.53) 3.46 (1.42-11.07) 1.44(0.53-3.36)
fat (%I
concn (ng/g of fat)
BCF
2.6 (0.6) 3.0 (0.9) 2.3 (0.6)
1440 9100 35 900
2050 7580 4170
3.3 (0.7)
6700
5150
Figures within parentheses refer to range. In the middle section of the table, concentrations of LPCB in fish ingig of fresh weight) are given for different stations (geometrical means, n = 10) as well as the percentage of fat (mean, n = 10, SD within parentheses). The calculated BCFs were based on the quotient of XPCB in fish (ng/g of extractable fat) to LPCB in water (ng/L) for the corresponding stations. a
Water
concentration ( n g / t )
0 transport
-50
0
50
Distance
Fish
(ngN
(ng/g f.w.1
Upstream
(g/day)
100
(km)
Downstream
012.
2s
7
1
FIGURE2. Concentration of XPCB (ng/L) in the water and the transport of PCB (dday) versus the distance from the source, Lake JUrnsjUn (0 km). Geometrical means of 10 samples.
Results The content of PCB in the river EmAn water was strongly influenced by the contaminated sediments in Lake JWsjon. The concentration of total PCB (the sum of all domains) in the outflowing water of Lake Jtirnsjon (no. 5) was 8.6 ng/L, and in the downstream location no. 6 it was 5.1 ng/L. This was significantly (t-test p 0.01) higher than the upstream locations no. 2, 0.7 ng/L, and no. 4, 1.2 ng/L (Table 2). The PCB concentration decreased with the distance from the source and so did the PCB transport (Figure 2). The composition of PCB domains in water and fish samples from different stations in the river EmAn is shown in Figure 3. The PCB composition in water from Lake Jtirnsjon (no. 5) was similar to the two stations, nos. 6 and 8, downstream (onlyno. 8 shownin the figure). The pattern resembled the low chlorinated commercial mixture Aroclor 1242, a pattern also seen previously in the contaminated sediment of Lake JWsjon (1). The patterns in the two upstream locations, nos. 2 and 4 (onlyno. 2 shown in Figure 3) were different and more highly chlorinated. A cluster analysis (Figure 4) showed the relationships between the patterns of PCB domains in water for the five stations. Because the water samples were taken over a long time (10 samples in 3 months), the changes in domain pattern over time had to be calculated to check ifthe samples could be evaluated together as a mean. The relative concentration among most of the domains did not differ over the investigated time span. However, for domains 4 and 16, the relative concentration increased in the autumn. The PCB burden from the contaminated sediments was also reflected in fish. In Lake Jtirnsjon, the total PCB 2012
ENVIRONMENTAL SCIENCE & T E C H N O L O G Y / VOL. 29, NO. 8, 1995
Domain
Domain
FIGURE 3. Pattern of PCB domains in water and fish from three corresponding sampling stations. No. 5 is Lake Jlrnsjlln. Upstream is nos. 2 and 1, and downstream is nos. 8 and 7, for water and fish, respectively. From left to right on the x-axis, ranging from low to highly chlorinated, domain nos. 1, 2, 3, 4, 6, 7, 8, 11, 13, 14, 15, 16, 19, 20, 21, 23, 24. 25, 27, 30, 31, 32,34. 38,39, 42. 43. 46, 47, 50, 53, 54.55,58,61,62,63,66,67,68,72,77,79,80,82, and 84 Geometrical means of 10 samples. Note the different y-axis scales.
concentration in fish was 825 ng/g (fresh weight), and this was significantly (t-test p < 0.01) higher compared with fish from all other sampling areas (Table1). At the upstream station no. 1, the PCB content in perch was 37 ng/g. The concentration on a fat weight basis for perch in Lake Jarnsjon was 36 pg/g of fat compared with 1.4 pg/g of extractable fat for fish at station no. 1. Generally, the PCB domain composition was more highly chlorinated in the fish than it was in the water (Figure 3 ) . This was clearly seen in the two upstream locations, nos. 1 and 3. In fish from the two lakes, Jarnsjon (no. 5) and no. 7 , which both are influenced by the low chlorinated PCB mixture, the composition of the domains was not as highly chlorinated as at the upstream locations. The BCFs for CPCB [calculated as the concentration in fish (ng/g of extractable fat) divided by the concentration in water (ng/L)] varied between the different locations ('Table 2). BCFs for some domains ranging from low to highly chlorinated resulted in a bell-shaped curve (Figure 5). BCFs of low chlorinated domains were less than these of highly chlorinated. However, above a certain degree of chlorination the BCF was reduced. The trend was seen at
water sampling
4 1
stations
EP56
O J 4
5
6
7
8
9
log Kow I
0.200
0.000
Distance FIGURE 4. Clusler analysis (single-linkage cluster, distances are 1-Peaman correlation coefficients) ofthe PCB composition in water from different stations in river EmBn. The longer the distance to a connection. the greater the degree of deviation in PCB composition between stations. Consequently. PCB composition at station nos. 5 and 6 show similsrily but not nos. 6 and 4. Geometrical means oflOwatersamplesfmm eachstation,which werethen standardized, were used.
0 Y
k!
30 20
10 0 4
11 14
16
20
31
39
58 62
72
77
79
84
Domain FIGURE 5. BCF versus some chosen PCB domains for the four correspondingstations offish and water samples IlR W4. W. 713). The bioconcentrationfactor, BCF.was calculated asthe geometrical mean of the PCB concentration in the 10 fishes (nglg of extractable fat) divided with the geometrical mean of 10 water samples ( n o ) .
all locations but was most pronounced for station no. 3 and Lake J h s j o n (no. 5). In these lakes, the highest concentrations of PCB in fish were recorded. When the domain numbers were translated into log&.F values and plotted versus log BCF for individual fish in Lake J h s j i i n (no. 51,log BCF increased over the log &F scale to about 7,after which log BCFs decreased (Figure6).
Discussion The contamination in river EmAn is of low magnitude compared with other contaminated river systems such as the Hudson River and the SchiawasseeRiver in the United States and river Seine in France (I). The concentrations in Hudson River water were reponed to be about 1 pg/L and in fish were 10-100 pg/g (fresh weight, 18). The results can be compared with data from Lake J h s j o n with PCB concentration in water of about 9 nglL and in fish of about 1 pg/g (fresh weight). The concentration of PCB declined with distance from the source (Lake J h s j o n ) . This can be attributed to the dilutiondue to increasingwater discharge downstreambut also due to PCB adsorption to particles that sediment in areas of lower flowvelocities. PCB will also be taken up by biota and subjected to abiotic and biotic degradation.
FIGURE6. Log BCFfmmbke J U m s j U n l ~ t i o n n o . 5 ~ v e ~ u s l o g ~ BCF values from the concentrations of a PCB domain (ng/g of fat) in 10 fishes divided by the geometrical mean ( n = 10) of the concentration in water. This is in order to get a measure of the range of values within fish. The domain numben were translated to log K, values (lfl. When more than one congener was present in a domain. a mean Kwwas calculated.
The domain pattern in Lake J h s j o n swater and in the two downstream stations nos. 6 and 8 resembles the low chlorinated commercial mixture Aroclor 1242, a pattern also seen earlier in the contaminated sediment of Lake J h s j o n (1). PCBsinthesedimentofthelakethusinnuence concentration downstream. The PCB pattern for the upstream station no. 2 resembles that in airborne fallout, indicating “background contamination (19). The proportion ofthe domains inthewater didnot difFer over the investigated time span for most of the domains. For domains4 and 16, however, the relative concentration increased in the autumn. This could be an effect of temperature, both direct-as they are low chlorinated and volatilize from water to air more easily when the temperature is high (ZO-and indirect, as the degradationincreases with temperature due to enhanced microbiological activity, especially for the low chlorinated congeners (21). One-year-old perch feed mainly on zooplankton, both in pelagic and benthic habitats. They are thus subjected to uptake from both sediment and water. It has been proposed that juvenile fish reflect to a higher degree than adult the concentrations of PCB in the water (18.22), while uptake of PCB from food is more important in older fish. The influence of the PCB-contaminated sediment in Lake J&nsjon was apparent, as concentrations were about 20 timeshigherinperchfromthislakethanfromtheupstream reference area. As shown in various studies (12,23, differences in concentrations of pollutants in fish may be due to age and sex. However, in this studythis is ruled out by the fact that all fish were of the same age and that the same number of females and males were chosen for each location. Contradictory to the hydrophobicity model (lo),fish at the differentlocationshad differentBCFs. Predictions from laboratory studies forecast the same BCFs. At locations subjected to higher PCB contamination, BCFs in fish were higher. If the uptake can be more accurately described by the more complicatedbioaccumulation models (13).several ecological explanations can be involved. The habitat and niche for the fishes may differ between the locations. The food chain structure has been shown to iniluence PCB content in fish and thus BCF (24). Barron (10)concluded that the observed concentration dependence of BCFs for hydrophobic molecules presumably is caused by saturation in processes that control adsorption, desorption, and elimination. MacDonald et al. (23 found differences in VOL. 29.
NO.8. 1995 1 ENVIRONMENTALSCIENCE &TECHNOLOGY
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BCFs with lake maximum depth which probably emanated from differences in food web structure. Larsson et al. (1) suggest that the direct uptake from water may be dominating in earlylife stages, whereas uptake from food dominates in adult fish. This is further stressed by the fact that contamination load within an organism increases with age (12,231. Opperhuizen (26)on the other hand means that the uptake from water via the gills is predominant. The constant large transfer of water across the gdls compared with the amount of ingested food will result in a higher uptake from water. This is more pronounced for small fish as the relative ventilationvolume decreases with increasing fish weight. For extremely hydrophobic chemicals however, the uptake from food may become more dominant. PCB and especially the highly chlorinated congeners may be regarded as extremely hydrophobic. The bell-shaped form of the curve between BCF and the different PCB domains, arranged with increasing number and thus lipophilicity and size, could be given several explanations. BCF has been shown to increase with increasing molecular weight (27). This is probably due to rising liphophilic character as the organic molecules increase in size. It can also emanate from the fact that low chlorinated congeners are metabolized within the fish to a greater extent than are the more chlorinated congeners (28). If &, is a correct measure for the uptake capacity, the relation between log BCF and log &, should show a direct proportionality. In most cases though, the deviation is large and indicates a more complex uptake, involving uptake from food, metabolism, excretion, etc. (29). The deviation may also depend on the difference in the characters of octanol and fat, i.e., the different solubility of pollutants in these media (28, 30). Why did the BCFs decrease at the highest domain numbers? It could be an effect of solubility and thus K,,. Chiou (28) compared pollutant solubility in octanol with the solubility in trilolein (glycerol trioleate). When the partitioning coefficient for octanollwater was plotted against the partitioning coefficient for triloleinlwater,there was a direct proportionality up to a log KO, of about 6, above which the curve deviated. The explanation given by Chiou is that &, values are difficult to measure for very lipophilic compounds. The decreasing BCF for chemicals with log KO, > 6 is described in laboratory studies with sediment and benthic invertebrates (31, 32, 6). For fish, Connel and Hawker (33)report a parabolicrelation between BCF and log KO, with a maximum log KO, of 6.7. Sugiura et ai. (34) report that accumulation of a chemical by fish decreases with increasing KO, for log KO, > 6. In a field study by Swackhamer and Hites (91, the effect is indicated, but only a few chemicals with high log &, were studied. The fat quality of an animal could play a role for the uptake, as the very hydrophobic molecules dissolve to a less extent in more polar fat (like phospholipids). Swackhamer and Hites (9) have suggested that differences in uptake between species could be explained by lipid composition, i.e., the relative amounts of saturated and unsaturated fatty acids. The composition of polar and nonpolar lipids in fish fat were shown to affect the partitioning abilityto PCBs in an experiment performed by Ewald and Larsson (35). Time is an important parameter for the relation between BCF and log KO, (33). The uptake rate increases with log KO,, but above a certain value the uptake rate decreases. 2014
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29. NO. 8.1995
If the compounds in fish have not reached a steady state, it would seem as if the BCFs were lower for the pollutants with high log &, (36, 33). In our investigation,the fishes were 1-year-old and thus supposed to have reached equilibrium. The weight of 1-year-oldperch is < log, and equilibrium for goldfish weighing 5 g is reported to be reached in 5-30 days (37). More complicated bioaccumulation models however indicate a longer time (38). BCFs variation over the &, range may also be an effect of reduced bioavailability since very hydrophobic compounds are sorbed to particles. Compounds with high IC, values bind to particles and are not available for direct uptake (39). When the pollutants are ingested with the food, they can sorb to sediment particles (often present) within the guts thereby preventing uptake (40). Another explanation is size exclusion. Molecular size is positively correlated with lipophilicity,and the molecules may be too big to pass the biological membranes. A limit of 0.95 nm for the molecules cross section and a length of 5.3 nm has been proposed (41, 261.
Acknowledgments We would like to thank A. Helg6e and B. Troedsson for valuablefield work. This work was financed by the Swedish National Protection Board (Lake JLnsjon Project).
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I I
Received for review N o v e m b e r 17, 1994. Revised manuscript received April 17, 1995. Accepted April 20, 1995.@
ES940707, @Abstractpublished in Advance ACS Abstracts, June 1, 1995.
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