Trophic-Leve Differences in Bio Concentration

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Environ. Sci. Techno/. 1995, 29, 154-160

Trophic-level Differences in theBioconcentrrrtion of Chemicals:Implications in AssessingEnvironmental BiomagdicationGERALD A . L E B L A N C *Department of Toxicology,P. .Box 7633,North CarolinaState University, Raleigh, North Carolina 27695

The occurre nce of elevated residue levels of variousxenobiotics with increasing trophic level has beendemonstrated in a variety of aquatic environments. Thisphenomenon is often cited as evidence of food chai nbiomagnification. However, studies of thebioconcentration of these chemicals (accumulationdirectly from the aqueous environment) with rep-resentatives of various trophic levels demonstrate tha tincreased bioconcentration o ccurs with increasingtrophic level. These species differences in biocon-centration can be miscons trued as biomagnification.Trophic-level differences i n bioconcentration are duelargely to increased lipid content and decreasedchemical elimination efficiency of organisms occupyin gincreasin g trophic levels. Slight biomagni fication(Le., 114 OD0 or a log P of >6.3. An equation isprovided with wh ich trophic-level differences inbioconce ntration can be estimated. These differencesmust be considered when assessing the potentialoccurrence of biomag nification.

154 ENVIRONMENTAL SCIENCE &TECHNOLOGY I VOL. 29, NO. 1. 1995

IntroductionThe concept of chemical biomagnification, the food chaintransfer of a chemical resulting in elevated concentrationsof the chemical with increasing trophic level, was popular-ized approximately three decades ago in response to theobserved demise of many raptor populations due to theaccumulation of DDT by these organisms. Analyses ofwhole organism DDT concentrations within a definedhabitat revealed a gradient of DDT concentrations, withrepresentatives of higher trophic levels containing thegreatest concentrations of DDT (e.g., Table 1). Thisconcentrative process was attributed to the presumedefficient transfer of DDT from one trophic level to the nextand the reduced biomass associatedwith each progressivetrophic level (1). That is, if the total amount of DDTcontained at one trophic level is efficiently transferred tothe next, and this next trophic level has less biomassassociated with it, then the concentration (but not the totalamount) of DDT associated with this trophic level will begreater than that present in the previous trophic level.Studies of the trophic-level distribution of other currentenvironmentally relevant contaminants, including PCBs(2,3) and dioxins (41, have led to the conclusion thatbiomagnification of lipophilic chemicals is a major con-tributor to the accumulation of chemicals in organismsoccupying higher trophic levels.

Order of magnitude differences in concentrations of achemical are often encountered among aquatic organismsoccupying the same habitat but at different trophic levels,implying significant biomagdication (e.g., Table1). How-ever, laboratory studies of the biomagnification processhave repeatedly (5-10) demonstrated the food chain (Le.,trophic) transfer of chemicals, but with little or no bio-magnification at steady-state equilibrium (Table2 ) . Theseobservations have led some to conclude that biomagnifi-cation is unlikely to occur with most chemicals and, relativeto bioconcentration (Table2) , is an insignificant source ofchemical bioaccumulation (5, 11) . [In the context of thisarticle, bioconcentration is defined as the uptake of achemical by an organism directly from the abiotic environ-ment, resulting in a concentration of chemical in theorganism that is higher than the environmental concentra-tion. Bioaccumulation is defined as the uptake of achemical by an organism directly from the abiotic and/orbiotic (Le., food) environment. The concentration ofchemical attained in the organism may or may not exceedthe concentration n the source.] Acceptance of the conceptof biomagnification is further confounded by the generallack of an adequate mechanistic model that would supportthe occurrence of biomagnification.

Biomagnification models generally assumed that thisprocess occurs via the same mechanism as bioconcentra-tion. Bioconcentration occurs largely through passivediffusion of the chemical (I,?), and steady-state equilibriumis attained when the fugacityof the chemical in the organismequals that in the environment. Fugacity is defined as thepropensity of a chemical to leave the compartment it isassociated with for another compartment (13). For ex-ample, the fugacity associated with a lipophilic chemical

* Phone: (919)515-7404; FAX: (919)515-7169.

0013-936)(/95/0929-0154$09.00/0 0 1994 American Chemical Society


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TABLE 1Concentration of DDT Measured in OrganismsRepresenting Four Trophic levels Sampled from along Island Estuary ( 1 )

organisms DOT Imflg. whole body basis)'fish-eating birds 2 4 + 14fish 4.1 + 8.1invertebrates 0.3 + 0.07plankton 0.04

*Data ar e presentedas meanf tandard deviation where multiplespecies were analyzed.

TABLE 2Laboratoly Studies of Accumulation of Xenobioticsby Fish from Water and Foods

compound BAF.' BAFt refDDT 127000 1 .1 52.3.7.8-TCDD 39000 0.40 8.9endrin 6800 0.14 5pentachlorobenzene 5000 0.11 6 .7leptophos 750 0.020 5trichlorobenzene 183 0.068 5octachlorodibenzodioxin 85 0.034 10

Biaaccumulation actorswere derived from the ratio of chemicalconcentrations Ifishlwaterl at steady-state equilibrium. a Bioaceumu-lation factorswere derived from the ratio of chemical concentrationslfish/faodl at steady-state equilibriumpartitioningfrom anaqueousmedium (Le.,compartment)to an organic medium is high. If the fugacity of a chemicalin an organism exceeds that in the environment through,for example, dilution or degradation ofthe chemical in theenvironment, hen the chemicalwillpassively diffuse fromthe organism back to the environment until the concentra-tion of chemical again reaches steady-state equilibriumwith the environment. Because hioconcentration n aquaticorganisms is primarily dictated by the passive partitioningof the chemical between an aqueous (environment) andan organic (organism)compartment, he bioconcentrationfactor (BCF),he ratio of the concentration of a chemicalin an organism and in the environment a t steady-stateequilibrium, correlates well with the chemical's octanol-water partition coefficient(7,14-21). hould the foodchaintransfer of chemicals also occur by passive diffusion, thenno further uptake should occur when the concentration ofthe chemical in the consumer organism reaches steady-state equilibrium (Le., equal fugacity) with the foodorganism. Since lipids are the primary storage site oflipophilic chemicals, biomagnification would not he pre-dicted to occw f the lipid composition of the food organismand consumer is comparable. However, biomagnificationmay occur if the lipid content of the food organism is lessthan that of the consumer. Equilibrium partitioning willalso be occurring between the consumer and the aqueousenvironment in addition to partitioning between food andconsumer, thus further reducing the likelihood of bio-magnification.

Recent mechanistic models of biomagnification haveattempted to attribute biomagnification to the increasedfugacityofachemicalinafoodorganismas aconsequenceof digestion (22,23). ccording to this model, digestion/absorption of the food results in reduced mass and lipidcontent of the food, thus increasing the fugacity of thechemical n this compartment and, accordingly. increasing

300

250

200h000 15 0r1s.mLLu 100

50

algae invertebrate f i s hFIGURE1. Bioconcentrationof DOTbyaquatic organisms occupyingdifferem trophic levels. Individual whole body bioconcentrationfactors IBCFs) were derived from various literature sources(summarized in ref 24) and are presented as mean + standarddeviation ( n = 1 [algael. 9 [invertebrates], and 6 [lish]).its propensity to transfer from the food to the consumer(23). ndeed, the bioaccumulation of octachlorobenzenebygoldfishfromfoodwas shown to increasewithdecreasinglipid content of the food (6').

Ifthe lipidcontent oforganismsincreaseswithincreasingtrophic level, then biomagnification could occur throughpassive diffusion from the food organism to the consumerorganism irrespective of digestion. However, acceptanceof this concept, that biomagnification may occur due todifferences in lipid composition among trophic levels andaccordingly different fugacities with lipophilic compounds,dictates acceptance of an additional consideration thatwould further complicate deciphering the significance ofhiomagnificationin heenvironment. That is, ifthe fugacityof a ipophilic compound decreases with increasing trophiclevel due to lipid composition of the organisms within thetrophic levels, then for a specific lipophilic chemical,hioconcentration would be predicted to increase withincreasing trophic level. Thus, the question remains: Isthe increased accumulation of lipophilic chemicals inorganisms occupying higher trophic levels due to bio-magnification or does it reflect simple hioconcentration inorganisms that have greater lipid content?Trophic-level Differences in Bioconcentration ofXenobioticsDDT first spurred concern over the occurrence of hio-magnification hrough the food chain as discussed above.Review of laboratory assessments of the bioconcentrationof DDT by aquatic organisms demonstrates that fishaccumulate DDT from water to significantly greater con-centrations than do invertebrates or phytoplankton (Figure1) . This -30-fold difference in accumulation of DDTbetween fish and invertebrates is in general agreementwiththe difference in DDT levels measured between represen-tatives of these trophic levels in the Long Island estuarythat initially raised concern over biomagnification (Table

VOL. 29, NO. 1.1995IENVIRONMENTAL SCIENCE &TECHNOLOGY m 155


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15.0

12.5

10.0h000 7.5c5UV 5.0m

2.5

70 -60M -

algae invertebrate

Tf i s h

40-

20 -

FIGURE 2. Bioconcentration of dieldrin by aquatic organismsoccupying different trophic levels (251.1). The trophic-level increase in organochlorine insecticidebioconcentrationis not restricted to DDT. In acomparativeassessment of dieldrin bioconcentration by an alga (Scene-desmus obliquus),an invertebrate (Daphnia magna), anda fish (Poecilia reticukzta),Reinert (23observed a progres-sive increase in bioconcentration at steady-state equilibriumwith these representatives ofthree progressive trophic levels(Figure2). This general relationship is maintained whensimilar analysisis done witheither dieldrin or endrin usingbioconcentration factors derived from several speciessegregated into these three trophic levels (Figure 3).Analyses of bioconcentration factors derived with inver-tebrates and fish demonstrate that lipophilic organochlorinecompounds consistently concentrate from the aqueousenvironment to greater levels in fish than in invertebrates(Table3). These results demonstrate aprogressive increasein bioconcentration of organochlorine compounds withincreasing trophic levels.Mechanisms Responsible for Trophic-LevelDifferences in BioconcentrationOrganismLipid ContentIncreaseswithhereasingTmpbicLevel. Lipid content of representatives of three aquatictrophic levels, primary producers (phytoplankton), primaryconsumers (invertebrates),and secondary consumers (fish)were derived from the literature and are summarized inTable 4. Differences in average lipid content exist amongthese trophic levels with lipid content increasing withincreasing trophic level. Thus, the increase in bioconcen-tration of organochlorine compounds with increasingtrophic level may be due largely to the differences in lipidcontent of the organisms within these trophic levels.Accordingly, the bioconcentration of these chemicals tosteady-state equilibrium with the environmental concen-trations could be mistakenly construedas biomagnification.

Oliver and Niimi (30)examined the bioaccumulation ofPCBs from various organisms sampled from Lake Ontario.They observed a trend of increasing PCB concentrationwith increasingtrophic level and concluded that food chain

40-1 Ia algae invertebrate f i s h0X7vLL2 '"1

nkT

" algae invertebrate f i s hFIGURE 3. Bioconcentration of dieldrin (A) and endrin (6) byorganismooccupying differenttmphic levels. Individual wholebodybioconcentrationfactors(BCFs)were obtainedfromvarious literaturesourceslsummarized in re126)andarepresentedasmean +standarddeviation. For dieldrin. n = 3 [algael, 2 inveltebratesl,and3 [fish].For endrin, n = 4 [algael.1 linvenebratesl, and 4 [fish].TABLE 3Bioconcentration Factors (BCF) for OrganochlorineXenobiotics with Fish and Invertebratesa

xenobiotic log P organism BCF rs lchlordane 6.00 f ish 37 800 27hexachlorobenzene 5.23 f ish 29 600 28Aroclor 1254 6.30 fish 49 050i 383 29Aroclor 1242 5.58 fish 274000 29

invertebrates 5 200invertebrates 13 900invertebratesinvertebrates 36 000

4 050 i 507

When several BCFswerefound n the literature. thesevaluerwereaveragedan d are presentedas mean f tandard deviation.transfer of PCBs resulted in significant biomagnification.The average PCB concentrations in the fish species exam-ined (2100ng/g wet weight) was 5-fold greater than averagelevels measured in invertebrates, (428 ng/g wet weight).This difference in the concentrationof PCBs is actually less

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TABLE 4Lipid Content (on Wet Weight Basis) of AquaticOrganisms Occupying Three Different GenericTrophic levels

organisms % lipide nb refphytoplankton 0.5c 1 30invertebrates 1.8i~ .90 8 24,30,52fish 5.4& 1.9 10 24,26,27,29,30

Mean f tandard deviation. n values represent the number ofspecies used in the % lipid determination. Only one lipid value on awet weight basis could be found for phytoplankton. Lipid content ofphytoplankton s typically measured on a dryweight basis(-10% lipid,dry weight). A lipid content of 0.5% on a weight wet basis s consistentwith measured lipid contents on a dry weight basis of 10% for singlecellular organisms that are -95% water.

n0)\0)Cvmx

5000

4000

3000

2000

1000

@ /OW I 9 I I I .0 2 4 6 8 10 12

Lipid (%)FIGURE 4. Relationship between lipid content of various organismssampled from Lake Ontario and whole body PCB concentration.Data derived from ref 30.than the trophic-level differences in the accumulation ofPCBs from the aqueous environment measured in labora-tory assessments of bioconcentration of these compoundsflable 3). Thus, trophic-level differencesin the accumula-tion of PCBs observed in the environment can be attributedto bioconcentration without having to consider any sig-nificant contribution by biomagnification. Furthermore,a strong relationship ( r = 0.92) exists between the con-centration of PCBs accumulated by the Lake Ontarioorganisms and their lipid content (Figure4).Accordingly,the trophic-level increase in concentration of PCBs by theseorganisms can be attributed largely to increased lipidcontent with increasing trophic level.

The relationship between bioconcentration and lipidcontent depicted in Figure4 is not preciselylinear. Rather,salmonids (data point representing the species with thegreatest lipid content) accumulated more PCB than wouldbe predicted by lipid content alone. Oliver and Niimi (30)attributed this increased accumulation of PCBs in LakeOntario salmonids to biomagnificationby these organisms.However, a similar trend with fish accumulating morechemical than predicted is evident when bioconcentration

data presented in Figures 1- 3 are compared to averagelipid content of representatives of the three trophic levelspresented in Table4. These observationssuggest that somefactor@), n addition to lipid content, contribute(s1 to theincreased accumulation of lipophilic chemicals at highertrophic levels and that this increased accumulation isindependent of biomagnification.

Chemical Depuration Rates DecreasewithIncreasingTrophic Level. The bioconcentration of a chemical isdictated by the rate at which the chemical is taken up bythe organism and the rate at which it is eliminated. Anincrease in uptake rate with no commensurate change inelimination rate or a decrease in elimination rate with nochange in uptake rate by species occupying higher trophiclevels would both result in increased bioconcentration ofchemicals by these organisms. Passive diffusion is likelythe primary mode of uptake and elimination of lipophilicenvironmental chemicals by unicellular organisms (Le.,phytoplankton). The large surface area across whichdiffusion occurs relative to organism mass allows for theconcentration of chemical within the organism to at tainsteady-state equilibrium with the environmental concen-tration very rapidly (e.g., ref 11). Under these conditions,the processes governing uptake and elimination are identi-cal (i.e., diffusion across the cell surface membrane).

As an organisms mass increases, the ratio of surfacearea to body mass decreases (11),and specialized mem-brane structures are required for effective uptake andelimination. In fish, gills are primarily responsible for theuptake of lipophilic chemicals from the aqueous environ-ment (31,32).Uptake across the gdls is dictated primarilyby passive diffusion (12).Accordingly, the rate of transportof chemicals across gill membranes correlates well withthe chemicals octanol-water partition coefficient (33).

Absorbed lipophilic chemicals are distributed, in as-sociation with serum binding proteins (341, to lipidcompartments within the body. Here, these chemicals aresequestered due to their low fugacity within these com-partments. Elimination from these compartments largelyentails reassociation of the xenobiotic with serum bindingproteins and transfer from the binding protein to theexcretory organs such as the liver. Liver cells (hepatocytes)contain specialized membranes (apical)across which manysuch chemicals are transported into the bile duct forelimination. This membrane encompasses a small per-centage of the total hepatocyte membrane (35) makingpassive diffusion across the membrane an inefficient meansof xenobiotic elimination from the body. In order tocompensate for this inefficiency, this membrane is equippedwith transport proteins that actively eliminate somechemicals from the body (35).For example, some xeno-biotic conjugates of glutathione and glucuronic acid areactively eliminated from the liver by the multispecificorganic anion transporter (35);while, unmetabolizedbenzo-[alpyrene and benz[alanthracene are eliminated by thetransporter P-glycoprotein (36, 37). P-glycoprotein hasbeen detected in both aquatic invertebrates and vertebrates(38-41).Manyxenobioticsmay not be recognizedby thesetransport proteins and may rely upon passive diffusion forelimination. Because of the sequestration of lipophilicxenobiotics in compartments distant from the site ofelimination and the reduced ratio of elimination sites:bodymass, elimination rates for lipophilic xenobiotics would beexpected to decrease with increasing body mass. Thishypothesis is substantiated in Figure 5, which illustrates

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3 4 5 6 7Lo g P

FIGURE 5. Relationshipsbetween chemical lipophilicity (log4 nddepuration rate (4) ith fish (squares) and daphnids (circles). Datafor fish and daphnidswer e obtained from ref42 and 43, respectively.the differences in chemical depuration rates between fishand invertebrates (daphnids). These results demonstratethat (a) depuration rates in both fish and daphnids areinverselyrelated to the lipophilicity (l og o ofthexenobiotic;(b) daphnids depurate xenobiotics approximately 10- 100times more rapidly than fish; and (c) differences indepuration rates between daphnids and fish increase withincreasing lipophilicity of the xenobiotic. Increased depu-ration rates by other invertebrates as compared to fish alsohave been demonstrated for individual chemicals includingkepone ( 4 4 ) and PCBs (45-47). Depuration rates werecalculated for dieldrin for alga, daphnid, and fish usingaccumulation data by Reinert (25) and the equation

K2 = 0.693/t5,where K2 is the depuration rate and t50 is the time requiredto accumulate 50% of the concentration of chemicalattained at steady-state equilibrium (12). Consistent withthe hypothesis, algae depurated dieldrin more rapidlythandaphnids, and daphnids depurated dieldrin more rapidlythan fish (K 2- 0.139, 0.036, and 0.004 h-l, respectively).Algae have also been demonstrated to depurate a-hexachlo-rocyclohexane (48),DDT ( I ] ) ,andatrazine (11) ignificantlymore rapidly than daphnids. This inverse relationshipbetween depuration rates of lipophilic chemicals andorganism mass would contribute to trophic level differencesin the bioconcentration ofxenobiotics andwouldcontributeto the appearance of environmental biomagnification.Summary and ConclusionEnvironmental biomagnification of a variety of chemicalshas been reported over the past three decades. However,laboratory experiments aimed at detecting and quantifymgbiomagmfication have largely confirmed he trophic transferof chemicals but with no biomagnification. Regressionanalyses of the bioaccumulation data presented in Table2 demonstrate a significant( r= 0.998) relationship betweenbioaccumulation from water and food (Figure6) . However,

1.21

0.0 0 30 60 90 120 150BAF, (X1000)

FIGURE 6. Relationship between he bioaccum ulation of chemicalsfrom 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 bioconcentrationfactorof > 114000. Few chemicals have been experimentallyshown to have BCFs > 114 000. For those chemicals (Le.,DDT, some PCBs),bioconcentration factors are in the orderof 1-2 x lo 5 (3,5,15).According to the regression equationderived from the experimental data in Figure 6, thebiomagnification of these compounds from one trophiclevel to the next would not exceed a factor of 2. This standsin striking contrast to the order of magnitude level ofbiomagnification between trophic levels predicted by somefood chain transfer models (49).Using the established (1 )relationship between bioconcentration factors (BCF) andoctanol-water partition coefficients Wow) of BCF =0.048(&,), results from the present study indicate that onlycompounds with a &, of > 2 x lo 6 would have thepropensity to biomagnify. This value is appreciably greaterthan previous estimates of lo5as being the lower limit ofKO, of chemicals susceptible to biomagnification (49,501.

The bioaccumulation model described by Thomann (50,51) represents an exemplary attempt to predict the foodchain transfer of chemicals. The model predicts that foodchain transfer of high logP chemicals contributes signifi-cantly to bioaccumulation in top predator organisms.Similarly, the present analyses indicates that, over a fourtrophic-level food chain, significant biomagnification mayoccur with high log P chemicals. However, the presentanalyses indicate that the majority of this trophic-leveldifference in biomagnification is attributed to trophic-leveldifferences in lipid content, while in the Thomann model,the trophic-level differences are observed following lipidnormalization. Thus, the present analyses are considerablymore conservative with regard to the extent of biomagni-fication that a chemical may undergo in the aquaticenvironment.Laboratory investigations of bioconcentration haveconsistently demonstrated that the bioconcentration factorsfor lipophilic chemicals are higher inorganisms that occupyhigher trophic levels. Results from the present study

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FIGURE 7. Relationship between chemical o ctano lhater partitioncoefficients (log p) and the ratio of fish and invertebrate biocon-centration factors (BCF). Data used are presented in Table 3 andFigure 3.demonstrate that this increased bioconcentration can beattributed to increased lipid concentration and decreasedchemical elimination efficiency associated with organismsoccupying increasing trophic levels. The increased lipidconcentration associated with organisms of increasingtrophic level provides a greater storage capacity for lipo-philic chemicals, resulting in higher BCFs at steady-stateequilibrium. In addition, as the mass of an organismincreases, chemical compartmentalization within the or-ganism increases and the ratio of depuration sites tochemical storage capacity of the organisms decreases.Accordingly, depuration rates for lipophilic chemicalsdecrease with increasing organism size. The increasedchemical storage capacity and slower chemical depurationrates in larger organisms can result in the appearance ofenvironmental biomagnification, when in actuality, thesedifferences represent species differences in bioconcentra-tion. Analyses of the ratios of bioconcentration factors forfish and invertebrates for several compounds presented inthis study (Table 3, Figure 3) demoiistrate that this ratioincreases linearly with increasing log P of the chemicals(Figure 7) and that bioconcentration factors for fish andinvertebrates would be the same for chemicals having a logP of 55.0. Using the regression equation derived fromFigure 7, the bioconcentration factor of chemicals havinga logP of '5 for invertebrates can be calculated from thatof fish using the following equation:

Chemical residue values can also be used in this equationin place of bioconcentrationfactors when the latter are notknown. Residue data summarized from Table1and Figure4 were used to assess the application of this equation tocalculate trophic-level differences in bioaccumulation ingeneral (i.e., not only between invertebrates and fish). Inthese examples, the chemical residues in fish were used tocalculate the chemical residues for the other trophic levels.

TABLE 5Comparison of DDT (Table 1) and PCB (Figure 4)Residues Measured in Organisms OccupyingDifferent Trophic lev els and Calculated ResiduesUsing Equation Presented in TexP

residue (mg/kg)chemical log P trophic level measured calculated

DDT 5.98 fish 4.1invertebrates 0.3 0.4plankton 0.04 0.03invertebrates 0.4 0.2plankton 0.03 0.03PCB 6.30b fish 2.1

a Fish residuevalueswere usedto calculatevaluesfor representativesof the other trophic levels. bThe og Pvalue or Aroclor 1254was usedin the calculation since this PCB was the most abundant formulationfound i n the organisms (30).Measured residue values presented arethe average residues of the various organisms analyzed from thedifferent trophic levels.

For these lipophilic materials (DDT and PCBs), bioaccu-mulation of the xenobiotics was correctly estimatedwithina factor of 2 (Table 5) . These results suggest that the aboveequation may have utility in assessing general trophic-leveldifferences in bioconcentration and warrant expansion ofthe equation to

-BCFlower trophic level - CFhigher aophic levell [(log (8.2)- 0iAdditional assessments using organisms representing avariety of trophic levels and compounds of varying lipo-philicities are necessary to validate this proposed relation-ship. Should the relationship hold true, then its use wouldsignificantly refine the modeling of the trophic-level bio-accumulation of xenobiotics, would help differentiatebetween the occurrence of bioconcentration versus bio-ma wc at ion of xenobiotics in the environment,and wouldstrengthenecological risk assessments of chemical for whichlimited experimentally determined bioconcentration dataare available.Literature Cited

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(10) Muir, D. C. G.; Yarechewski, A. L.; Knoll, A.; Webster, G. R . B.Environ. Toxicol. Chem. 1988, 5, 261-272.(11) Ellgehausen, H. ; Guth, J. A. ; Esser, H . 0.Ecotoxicol. Environ. Suf:(12) Spacie,A.; Hamelink,J. L. In Fundamental ofAquatic Toxicology;Rand, G .M., Petrocelli,S. R ., Eds.; Hemisphere Publishers: Ne wYork, 1985; pp 495-525.

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(13) Clark, T.; Clark, K.; Paterson, S.; Mackay, D.; Norstrom, R. J.(14) Chiou, C. T.; Freed, V. H.; Schmedding, D. W.; Kohnert, R. L.(15) Veith, G. D. ;DeFoe, D. L.; Bergstedt, B. V.J. Fish. Res. Board Can.(16) Kanazawa, J. Pestic. Sci. 1981, 12, 417-424.(17) Mackay, D. Environ. Sci. Technol. 1982, 16, 274-278.(18) Davis, R. P.; Dobbs, A. J . WaterRes. 1984, 10, 1253-1262.(19) Chiou, C. T. Environ. Sci. Technol. 1985, 19, 57-62.(20) Hawker, D. W.; Connell, D. W. Water Res. 1988, 6, 701-707.(21) Hawker, D. W.; Co nn d, D. W. Environ. Sc i . Technol. 1989, 23,961-965.(22) Connolly,1. P.; Pedersen, C. J. Environ. Sci. Technol. 1988, 22,99-103.(23) Clark,K. E.; Gobas, P. C.; Mackay,D.Environ. Sci. Technol.1990,

24, 1203-1213.(24) U.S. EPA.Ambient W ater Quality Criteria orD DC OfficeofWaterRegulation and Standards Criteria: Washington, DC, 1980.(25) Reinert, R. E. J. Fish. Res. Board Can. 1972, 29, 1413-1418.(26) US. EPAAmbient Water Quality Criteria orAldrinlDieMrin andWater Quality Criteria for Endrin; Office o f Water Regulationand Standards Criteria: Washington, DC, 1980.(27) US. EPA Ambient Water Quality Criteria for Chlordane; Officeo f Water Regulation and Standards Criteria: Washington, DC,1980.(28) Schuytema, G. S.; Krawczyk, D. F.; Griffis, W. L.; Nebeker, A. V.;Robideaux,M.L.; Brownawell,B. J.; Westall,J. C.Environ. Toxicol.Chem. 1988, 7, 1035-1045.(29) US.EPA Ambient Water Quality Criteria for PolychlorinatedBiphenyls; Office o f Water Regulation and Standards Criteria:Washington, DC, 1980.(30) Oliver ,B. G.; Niimi, A. J. Environ. Sci. Technol. 1988, 22, 388-397.(31) Holden, A. V. Annu. Appl. Biol. 1962, 50, 467-477.(32) Hayton, W. L.; Barron, M. G. Environ. Toxicol. Chem. 1990, 9,(33) Maren, T. H.; Embry, R.; Broder, L. E. Comp . Biochem. Physiol.(34) Riviere . E. In Introdu ction to Biochemical Toxicology;Hodgson,E., Levi, P. E., Eds.; Appleton and Lange: Norwalk, CT, 1994, pp(35) LeBlanc, G. A. Chem.-Biol. Interactions 1994, 190, 101-120.

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143.Received for review April 26, 1994. Revised m anuscr ipt re-ceived September 16, 1994. Accepted September 19, 1994.@E59402622

@ Abstract published in AdvanceACSAbstracts, November 1,1994.

160 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 1, 1995

Trophic-Leve Differences in Bio Concentration

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