Environ. Sci. Techno/. 1995, 29, 154-160
Trophic-level Differences in the Bioconcentrrrtion of Chemicals: Implications in Assessing Environmental Biomagdication GERALD A . L E B L A N C * Department of Toxicology,P.0. Box 7633, North Carolina State University, Raleigh, North Carolina 27695
The occurrence of elevated residue levels of various xenobiotics with increasing trophic level has been demonstrated in a variety of aquatic environments. This phenomenon is often cited as evidence of food chain biomagnification. However, studies of the bioconcentration of these chemicals (accumulation directly from the aqueous environment) with representatives of various trophic levels demonstrate that increased bioconcentration occurs with increasing trophic level. These species differences in bioconcentration can be misconstrued as biomagnification. Trophic-level differences in bioconcentration are due largely to increased lipid content and decreased chemical elimination efficiency of organisms occupying increasing trophic levels. Slight biomagnification (Le., 114 OD0 or a log P of >6.3. An equation is provided with which trophic-level differences in bioconcentration can be estimated. These differences must be considered when assessing the potential occurrence of biomag nification.
Introduction The concept of chemical biomagnification, the food chain transfer of a chemical resulting in elevated concentrations of the chemical with increasing trophic level, was popularized approximately three decades ago in response to the observed demise of many raptor populations due to the accumulation of DDT by these organisms. Analyses of whole organism DDT concentrations within a defined habitat revealed a gradient of DDT concentrations, with representatives of higher trophic levels containing the greatest concentrations of DDT (e.g., Table 1). This concentrative process was attributed to the presumed efficient transfer of DDT from one trophic level to the next and the reduced biomass associated with each progressive trophic level (1). That is, if the total amount of DDT contained at one trophic level is efficiently transferred to the next, and this next trophic level has less biomass associated with it, then the concentration (but not the total amount) of DDT associated with this trophic level will be greater than that present in the previous trophic level. Studies of the trophic-level distribution of other current environmentally relevant contaminants, including PCBs (2, 3) and dioxins (41, have led to the conclusion that biomagnification of lipophilic chemicals is a major contributor to the accumulation of chemicals in organisms occupying higher trophic levels. Order of magnitude differences in concentrations of a chemical are often encountered among aquatic organisms occupying the same habitat but at different trophic levels, implying significantbiomagdication (e.g., Table 1). However, laboratory studies of the biomagnification process have repeatedly (5-10) demonstrated the food chain (Le., trophic) transfer of chemicals, but with little or no biomagnification at steady-state equilibrium (Table 2). These observations have led some to conclude that biomagnification is unlikely to occur with most chemicals and, relative to bioconcentration (Table 2), is an insignificant source of chemical bioaccumulation (5, 11). [In the context of this article, bioconcentration is defined as the uptake of a chemical by an organism directly from the abiotic environment, resulting in a concentration of chemical in the organism that is higher than the environmental concentration. Bioaccumulation is defined as the uptake of a chemical by an organism directly from the abiotic and/or biotic (Le., food) environment. The concentration of chemical attained in the organism may or may not exceed the concentration in the source.] Acceptance of the concept of biomagnification is further confounded by the general lack of an adequate mechanistic model that would support the occurrence of biomagnification. Biomagnification models generally assumed that this process occurs via the same mechanism as bioconcentration. Bioconcentration occurs largely through passive diffusion of the chemical (I,?), and steady-state equilibrium is attained when the fugacity of the chemical in the organism equals that in the environment. Fugacity is defined as the propensity of a chemical to leave the compartment it is associated with for another compartment (13). For example, the fugacity associated with a lipophilic chemical * Phone: (919)515-7404; FAX: (919)515-7169.
154 ENVIRONMENTAL SCIENCE &TECHNOLOGY I VOL. 29, NO. 1. 1995
0013-936)(/95/0929-0154$09.00/0
0 1994 American
Chemical Society
300
TABLE 1
Concentration of DDT Measured in Organisms Representing Four Trophic levels Sampled from a long Island Estuary ( 1 ) organisms
DOT Imflg. whole body basis)'
fish-eating birds fish invertebrates plankton
2 4 + 14 4.1 8.1 0.3 0.07 0.04
250
200
+ +
h
0 0
*Data are presented as mean f standard deviation where multiple
species were analyzed.
0
1s. LL
u
TABLE 2
Laboratoly Studies of Accumulation of Xenobiotics by Fish from Water and Foods compound DDT 2.3.7.8-TCDD endrin pentachlorobenzene leptophos trichlorobenzene octachlorodibenzodioxin
150
r
BAF.' 127000 39000 6800 5000 750
183 85
BAFt
ref
1.1
5 8.9 5 6.7 5 5 10
0.40
0.14 0.11 0.020 0.068 0.034
Biaaccumulationfactors were derived from the ratio of chemical concentrations Ifishlwaterl at steady-state equilibrium. a Bioaceumulation factors were derived from the ratio of chemical concentrations lfish/faodl at steady-state equilibrium
partitioningfrom anaqueousmedium (Le.,compartment) to an organic medium is high. If the fugacity of a chemical in an organism exceeds that in the environment through, for example, dilution or degradation ofthe chemical in the environment, then the chemical will passively diffuse from the organism back to the environment until the concentration of chemical again reaches steady-state equilibrium with the environment. Because hioconcentrationin aquatic organisms is primarily dictated by the passive partitioning of the chemical between an aqueous (environment) and an organic (organism)compartment, the bioconcentration factor (BCF),the ratio of the concentration of a chemical in an organism and in the environment at steady-state equilibrium, correlates well with the chemical's octanolwater partition coefficient (7,14-21).Should the foodchain transfer of chemicals also occur by passive diffusion, then no further uptake should occur when the concentration of the chemical in the consumer organism reaches steadystate equilibrium (Le., equal fugacity) with the food organism. Since lipids are the primary storage site of lipophilic chemicals, biomagnification would not he predicted to occw if the lipid composition of the food organism and consumer is comparable. However, biomagnification may occur if the lipid content of the food organism is less than that of the consumer. Equilibrium partitioning will also be occurring between the consumer and the aqueous environment in addition to partitioning between food and consumer, thus further reducing the likelihood of biomagnification. Recent mechanistic models of biomagnification have attempted to attribute biomagnification to the increased fugacityofachemicalinafoodorganismas aconsequence of digestion (22,23).According to this model, digestion/ absorption of the food results in reduced mass and lipid content of the food, thus increasing the fugacity of the chemical in this compartment and, accordingly. increasing
m
100
50
algae
invertebrate
fish
FIGURE1. Bioconcentrationof DOTbyaquatic organisms occupying differem trophic levels. Individual whole body bioconcentration factors IBCFs) were derived from various literature sources (summarized in ref 24) and are presented as mean standard deviation ( n = 1 [algael. 9 [invertebrates], and 6 [lish]).
+
its propensity to transfer from the food to the consumer (23).Indeed, the bioaccumulation of octachlorobenzene bygoldfishfromfoodwasshown to increasewithdecreasing lipid content of the food (6'). Ifthe lipidcontent oforganismsincreaseswithincreasing trophic level, then biomagnification could occur through passive diffusion from the food organism to the consumer organism irrespective of digestion. However, acceptance of this concept, that biomagnification may occur due to differences in lipid composition among trophic levels and accordingly different fugacities with lipophilic compounds, dictates acceptance of an additional consideration that would further complicate deciphering the significance of hiomagnificationintheenvironment. That is, ifthe fugacity ofa lipophilic compound decreases with increasing trophic level due to lipid composition of the organisms within the trophic levels, then for a specific lipophilic chemical, hioconcentration would be predicted to increase with increasing trophic level. Thus, the question remains: Is the increased accumulation of lipophilic chemicals in organisms occupying higher trophic levels due to biomagnificationor does it reflect simple hioconcentration in organisms that have greater lipid content?
Trophic-level Differences in Bioconcentration of Xenobiotics DDT first spurred concern over the occurrence of hiomagnification through the food chain as discussed above. Review of laboratory assessments of the bioconcentration of DDT by aquatic organisms demonstrates that fish accumulate DDT from water to significantly greater concentrations than do invertebrates or phytoplankton (Figure 1). This -30-fold difference in accumulation of DDT between fish and invertebrates is in general agreementwith the difference in DDT levels measured between representatives of these trophic levels in the Long Island estuary that initially raised concern over biomagnification (Table VOL. 29, NO. 1.1995IENVIRONMENTAL SCIENCE &TECHNOLOGY m 155
15.0
70 -
T
60 12.5
M10.0
I
40-1
h
0
0 0
7.5
c
5 U
V
m
5.0
a 0
2.5
algae
invertebrate
fish
7
X
v
fish algae invertebrate FIGURE 2. Bioconcentration of dieldrin by aquatic organisms occupying different trophic levels (251.
1). The trophic-level increase in organochlorine insecticide bioconcentrationis not restricted to DDT. In acomparative assessment of dieldrin bioconcentration by an alga (Scenedesmus obliquus),an invertebrate (Daphnia magna), and a fish (Poecilia reticukzta), Reinert (23 observed a progressive increase in bioconcentration at steady-state equilibrium with these representatives ofthree progressive trophic levels (Figure 2). This general relationship is maintained when similar analysisis done witheither dieldrin or endrin using bioconcentration factors derived from several species segregated into these three trophic levels (Figure 3). Analyses of bioconcentration factors derived with invertebrates and fish demonstrate that lipophilic organochlorine compounds consistently concentrate from the aqueous environment to greater levels in fish than in invertebrates (Table 3). These results demonstrate aprogressive increase in bioconcentration of organochlorine compounds with increasing trophic levels.
Mechanisms Responsible for Trophic-Level Differences in Bioconcentration
2 '"1
T
4020 -
n "
k algae
invertebrate
fish
FIGURE 3. Bioconcentration of dieldrin (A) and endrin (6) by organismooccupyingdifferenttmphic levels. Individual whole body bioconcentrationfactors (BCFs)were obtained from various literature sourceslsummarized in re126)andarepresentedasmean +standard deviation. For dieldrin. n = 3 [algael, 2 [inveltebratesl,and 3 [fish]. For endrin, n = 4 [algael. 1 linvenebratesl, and 4 [fish]. TABLE 3
Organism Lipid Content Increaseswith hereasingTmpbic Level. Lipid content of representatives of three aquatic trophic levels, primary producers (phytoplankton), primary consumers (invertebrates),and secondary consumers (fish) were derived from the literature and are summarized in Table 4. Differences in average lipid content exist among these trophic levels with lipid content increasing with increasing trophic level. Thus, the increase in bioconcentration of organochlorine compounds with increasing trophic level may be due largely to the differences in lipid content of the organisms within these trophic levels. Accordingly, the bioconcentration of these chemicals to steady-state equilibrium with the environmental concentrations could be mistakenly construedas biomagnification. Oliver and Niimi (30)examined the bioaccumulation of PCBs from various organisms sampled from Lake Ontario. They observed a trend of increasing PCB concentration with increasingtrophic level and concluded that food chain 156 m ENVIRONMENTAL SCIENCE &TECHNOLOGY IVOL. 29.
LL
NO. 1.1995
Bioconcentration Factors (BCF) for Organochlorine Xenobiotics with Fish and Invertebratesa xenobiotic chlordane
log P
organism
6.00 fish
BCF
37 800 5 200 hexachlorobenzene 5.23 fish 29 600 invertebrates 13 900 Aroclor 1254 6.30 fish 49 050 i 6 383 invertebrates 4 050 i 1 507 Aroclor 1242 5.58 fish 274 000 invertebrates 36 000
rsl
27
invertebrates
28 29 29
When several BCFswerefound in the literature. thesevaluerwere averaged and are presented as mean f standard deviation.
transfer of PCBs resulted in significant biomagnification. The average PCB concentrations in the fish species examined (2100 ng/g wet weight) was 5-fold greater than average levels measured in invertebrates, (428 ng/g wet weight). This difference in the concentration of PCBs is actually less
TABLE 4
Lipid Content (on Wet Weight Basis) of Aquatic Organisms Occupying Three Different Generic Trophic levels organisms
% lipide
nb
phytoplankton invertebrates
0.5c 1.8i~0.90 5.4& 1.9
8 10
fish
ref
1
30 24,30,52 24,26,27,29,30
Mean f standard deviation. n values represent the number of species used in the % lipid determination. Only one lipid value on a wet weight basis could be found for phytoplankton. Lipid content of phytoplankton is typically measured on a dryweight basis (-10% lipid, dry weight). A lipid content of 0.5% on a weight wet basis is consistent with measured lipid contents on a dry weight basis of 10% for single cellular organisms that are -95% water.
5000
4000
n
0) \ 0)
3000
C v
m
x
2000
1000
@ /
OW’ 0
I
2
’
9
4
’
I
’
6
I
8
’
I
10
.
I
12
Lipid (%) FIGURE 4. Relationship between lipid content of various organisms sampled from Lake Ontario and whole body PCB concentration. Data derived from ref 30.
than the trophic-level differences in the accumulation of PCBs from the aqueous environment measured in laboratory assessments of bioconcentration of these compounds flable 3). Thus, trophic-level differences in the accumulation of PCBs observed in the environment can be attributed to bioconcentration without having to consider any significant contribution by biomagnification. Furthermore, a strong relationship ( r = 0.92) exists between the concentration of PCBs accumulated by the Lake Ontario organisms and their lipid content (Figure 4). Accordingly, the trophic-level increase in concentration of PCBs by these organisms can be attributed largely to increased lipid content with increasing trophic level. The relationship between bioconcentration and lipid content depicted in Figure 4 is not preciselylinear. Rather, salmonids (data point representing the species with the greatest lipid content) accumulated more PCB than would be predicted by lipid content alone. Oliver and Niimi (30) attributed this increased accumulation of PCBs in Lake Ontario salmonids to biomagnificationby these organisms. However, a similar trend with fish accumulating more chemical than predicted is evident when bioconcentration
data presented in Figures 1-3 are compared to average lipid content of representatives of the three trophic levels presented in Table 4. These observationssuggest that some factor@),in addition to lipid content, contribute(s1 to the increased accumulation of lipophilic chemicals at higher trophic levels and that this increased accumulation is independent of biomagnification. Chemical Depuration Rates Decrease with Increasing Trophic Level. The bioconcentration of a chemical is dictated by the rate at which the chemical is taken up by the organism and the rate at which it is eliminated. An increase in uptake rate with no commensurate change in elimination rate or a decrease in elimination rate with no change in uptake rate by species occupying higher trophic levels would both result in increased bioconcentration of chemicals by these organisms. Passive diffusion is likely the primary mode of uptake and elimination of lipophilic environmental chemicals by unicellular organisms (Le., phytoplankton). The large surface area across which diffusion occurs relative to organism mass allows for the concentration of chemical within the organism to attain steady-state equilibrium with the environmental concentration very rapidly (e.g., ref 11). Under these conditions, the processes governing uptake and elimination are identical (i.e., diffusion across the cell surface membrane). As an organism’s mass increases, the ratio of surface area to body mass decreases (11),and specialized membrane structures are required for effective uptake and elimination. In fish, gills are primarily responsible for the uptake of lipophilic chemicals from the aqueous environment (31,32). Uptake across the gdls is dictated primarily by passive diffusion (12). Accordingly, the rate of transport of chemicals across gill membranes correlates well with the chemical’s octanol-water partition coefficient (33). Absorbed lipophilic chemicals are distributed, in association with serum binding proteins (341, to lipid compartments within the body. Here, these chemicals are sequestered due to their low fugacity within these compartments. Elimination from these compartments largely entails reassociation of the xenobiotic with serum binding proteins and transfer from the binding protein to the excretory organs such as the liver. Liver cells (hepatocytes) contain specialized membranes (apical)across which many such chemicals are transported into the bile duct for elimination. This membrane encompasses a small percentage of the total hepatocyte membrane (35) making passive diffusion across the membrane an inefficient means of xenobiotic elimination from the body. In order to compensate for this inefficiency, this membrane is equipped with transport proteins that actively eliminate some chemicals from the body (35). For example, some xenobiotic conjugates of glutathione and glucuronic acid are actively eliminated from the liver by the multispecific organic anion transporter (35);while, unmetabolizedbenzo[alpyrene and benz[alanthracene are eliminated by the transporter P-glycoprotein (36, 37). P-glycoprotein has been detected in both aquatic invertebrates and vertebrates (38-41).Manyxenobioticsmay not be recognizedby these transport proteins and may rely upon passive diffusion for elimination. Because of the sequestration of lipophilic xenobiotics in compartments distant from the site of elimination and the reduced ratio of elimination sites:body mass, elimination rates for lipophilic xenobiotics would be expected to decrease with increasing body mass. This hypothesis is substantiated in Figure 5, which illustrates VOL. 29, NO. 1, 1995 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
167
1.21
0.0
0
5
4
3
6
30
60
90
120
150
7
Log P FIGURE 5. Relationshipsbetween chemical lipophilicity (log 4and depuration rate (4)with fish (squares) and daphnids (circles). Data for fish and daphnidswere obtained from ref 42 and 43, respectively.
the differences in chemical depuration rates between fish and invertebrates (daphnids). These results demonstrate that (a) depuration rates in both fish and daphnids are inverselyrelated to the lipophilicity(logo ofthexenobiotic; (b) daphnids depurate xenobiotics approximately 10- 100 times more rapidly than fish; and (c) differences in depuration rates between daphnids and fish increase with increasing lipophilicity of the xenobiotic. Increased depuration rates by other invertebrates as compared to fish also have been demonstrated for individual chemicals including kepone ( 4 4 ) and PCBs (45-47). Depuration rates were calculated for dieldrin for alga, daphnid, and fish using accumulation data by Reinert (25) and the equation K2 = 0.693/t5,
where K2 is the depuration rate and t50 is the time required to accumulate 50% of the concentration of chemical attained at steady-state equilibrium (12). Consistent with the hypothesis, algae depurated dieldrin more rapidlythan daphnids, and daphnids depurated dieldrin more rapidly than fish (K2 0.139, 0.036, and 0.004 h-l, respectively). Algae have also been demonstrated to depurate a-hexachlorocyclohexane (48),DDT ( I ] ) ,andatrazine (11)significantly more rapidly than daphnids. This inverse relationship between depuration rates of lipophilic chemicals and organism mass would contribute to trophic level differences in the bioconcentration ofxenobiotics and would contribute to the appearance of environmental biomagnification.
-
Summary and Conclusion Environmental biomagnification of a variety of chemicals has been reported over the past three decades. However, laboratory experiments aimed at detecting and quantifymg biomagmfication have largely confirmed the trophic transfer of chemicals but with no biomagnification. Regression analyses of the bioaccumulation data presented in Table 2 demonstrate a significant ( r = 0.998) relationship between bioaccumulation from water and food (Figure6). However, 158 1 ENVIRONMENTAL SCIENCE &TECHNOLOGY / VOL. 29, NO. 1, 1995
BAF,
(X1000)
FIGURE 6. Relationship between the bioaccumulationof chemicals from water ( B A L ) and from food (BAF,). Bioaccumulation factors (BAF) used in this comparison are summarized in Table 2.
these data reveal that for a chemical to biomagnify (i.e., BMF > 11,the chemical must have a bioconcentrationfactor of > 114 000. Few chemicals have been experimentally shown to have BCFs > 114 000. For those chemicals (Le., DDT, some PCBs),bioconcentration factors are in the order of 1-2 x lo5 (3,5,15).According to the regression equation derived from the experimental data in Figure 6, the biomagnification of these compounds from one trophic level to the next would not exceed a factor of 2. This stands in striking contrast to the order of magnitude level of biomagnification between trophic levels predicted by some food chain transfer models (49). Using the established (17 ) relationship between bioconcentration factors (BCF) and octanol-water partition coefficients Wow) of BCF = 0.048(&,), results from the present study indicate that only compounds with a &, of > 2 x lo6 would have the propensity to biomagnify. This value is appreciably greater than previous estimates of lo5 as being the lower limit of KO, of chemicals susceptible to biomagnification (49,501. The bioaccumulation model described by Thomann (50, 51) represents an exemplary attempt to predict the food chain transfer of chemicals. The model predicts that food chain transfer of high log P chemicals contributes significantly to bioaccumulation in top predator organisms. Similarly, the present analyses indicates that, over a four trophic-level food chain, significant biomagnification may occur with high log P chemicals. However, the present analyses indicate that the majority of this trophic-level difference in biomagnification is attributed to trophic-level differences in lipid content, while in the Thomann model, the trophic-level differences are observed following lipid normalization. Thus, the present analyses are considerably more conservative with regard to the extent of biomagnification that a chemical may undergo in the aquatic environment. Laboratory investigations of bioconcentration have consistentlydemonstrated that the bioconcentration factors for lipophilic chemicals are higher in organisms that occupy higher trophic levels. Results from the present study
13
TABLE 5
11
Comparison of DDT (Table 1) and PCB (Figure 4) Residues Measured in Organisms Occupying Different Trophic levels and Calculated Residues Using Equation Presented in TexP
n
e, w
2 n
residue (mg/kg)
9
chemical
log P
trophic level
DDT
5.98
fish invertebrates plankton fish
measured
calculated
e,
tt e, >
C
7
7
PCB
r
6.30b
v)
55 L
a
0
4.1
0.3
0.4
0.03
invertebrates
0.04 2.1 0.4
plankton
0.03
0.03
0.2
Fish residuevalueswere usedto calculatevaluesfor representatives
of the other trophic levels. bThe log Pvalue for Aroclor 1254 was used in the calculation since this PCB was the most abundant formulation
m 3
found in the organisms (30).Measured residue values presented are the average residues of the various organisms analyzed from the different trophic levels.
1
5.0
5.2
5.4
5.6
5.8
6.0
6.2
6.4
Log ? FIGURE 7. Relationship between chemical octanolhater partition coefficients (log p) and the ratio of fish and invertebrate bioconcentration factors (BCF). Data used are presented in Table 3 and Figure 3.
demonstrate that this increased bioconcentration can be attributed to increased lipid concentration and decreased chemical elimination efficiency associated with organisms occupying increasing trophic levels. The increased lipid concentration associated with organisms of increasing trophic level provides a greater storage capacity for lipophilic chemicals, resulting in higher BCFs at steady-state equilibrium. In addition, as the mass of an organism increases, chemical compartmentalization within the organism increases and the ratio of depuration sites to chemical storage capacity of the organisms decreases. Accordingly, depuration rates for lipophilic chemicals decrease with increasing organism size. The increased chemical storage capacity and slower chemical depuration rates in larger organisms can result in the appearance of environmental biomagnification, when in actuality, these differences represent species differences in bioconcentration. Analyses of the ratios of bioconcentration factors for fish and invertebrates for several compounds presented in this study (Table 3, Figure 3) demoiistrate that this ratio increases linearly with increasing log P of the chemicals (Figure 7) and that bioconcentration factors for fish and invertebrates would be the same for chemicals having a log P of 55.0. Using the regression equation derived from Figure 7, the bioconcentration factor of chemicals having a log P of '5 for invertebrates can be calculated from that of fish using the following equation:
Chemical residue values can also be used in this equation in place of bioconcentrationfactors when the latter are not known. Residue data summarized from Table 1and Figure 4 were used to assess the application of this equation to calculate trophic-level differences in bioaccumulation in general (i.e., not only between invertebrates and fish). In these examples, the chemical residues in fish were used to calculate the chemical residues for the other trophic levels.
For these lipophilic materials (DDT and PCBs), bioaccumulation of the xenobiotics was correctly estimatedwithin a factor of 2 (Table 5). These results suggest that the above equation may have utility in assessing general trophic-level differences in bioconcentration and warrant expansion of the equation to BCFlower trophic level
- BCFhigher
aophic levell [(log
(8.2) - 40i
Additional assessments using organisms representing a variety of trophic levels and compounds of varying lipophilicities are necessary to validate this proposed relationship. Should the relationship hold true, then its use would significantly refine the modeling of the trophic-level bioaccumulation of xenobiotics, would help differentiate between the occurrence of bioconcentration versus biom a w c a t i o n of xenobiotics in the environment,and would strengthenecological risk assessments of chemical for which limited experimentally determined bioconcentration data are available.
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Received for review April 26, 1994. Revised manuscript received September 16, 1994. Accepted September 19, 1994.@
E59402622 @
Abstract published in AdvanceACSAbstracts, November 1,1994.
