Environ. Sci. Techno/. 1995, 29, 2555-2560
Bioconcentration of Polycyclic Aromatic Compounds from Sediments to Muscle of Finfish J O C E L Y N E HELLOU,*,+ DONALD MACKAY,' AND B R I A N FOWLERS Toxicology Section, Department of Fisheries and Oceans, P.O. Box 5667, St. John's, Newfoundland, AIC 5x1 Canada, Environmental and Resource Studies Program, Trent Uniuersity, Peterborough, Ontario, K9J 7B8 Canada, and Axys Analytical Services, P.O.Box 221 9, Sidney, British Columbia, V8L 3SI Canada
The uptake of polycyclic aromatic compounds (PAC) from contaminated sediments into the muscle of finfish is described and modeled. Winter flounder (Pseudopleuronectes americanus) were exposed to various concentrations of Hibernia crude oil in sediments during 4 months in the winter. Concentrations of parental and specific alkylated PAC, including polycyclic aromatic hydrocarbons (PAH) and a polycyclic aromatic sulfur heterocycle (PASH, represented by dibenzothiophene, DBT) were determined in sediments and muscle. Commercially available specific alkylated naphthalenes, phenanthrenes, and anthracenes with known aqueous solubilities were quantified. PAH concentrations in sediments ranged from those expected in pristine areas to levels 25-50 times higher. Biota-sediment accumulation factors (BSAF) were deduced, showing that the more watersoluble PAH displayed higher BSAFs. A simple fugacity model describing the equilibrium and kinetics of uptake of chemicals from sediment suggests that the more soluble PAH are approaching equilibrium. However, the less soluble higher molecular weight PAH require a much longer time to reach steady state because of their low concentration in water.
Introduction The bioconcentration of organic contaminants (concentration in tissue/concentration in water) has been described in terms of equilibrium partitioning, using the octanolwater partition coefficient (Kow),which relates water solubility and lipid affinity of hydrophobic and lipophilic compounds (1-3). The bioavailability of xenobiotics has also been discussed from the perspective of the effect of exogenous environmental variables (4, 5). * To whom correspondence should be addressed; e-mail address:
[email protected]. Department of Fisheries and Oceans. Trent University. 5 A x y s Analytical Services. +
0013-936W95/0929-2555$09.00/0
0 1995 American Chemical Society
Polycyclic aromatic compounds (PAC),including polycyclic aromatic hydrocarbons (PAH)and sulfur heterocycles (PASH)tend to sorb to particulates and become deposited in sediments where their concentration can be more easily determined than in water (6). However, the observed presence of PAC in sediments needs to be translated into bioavailability and future bioaccumulation in biota and ultimately into effects. The presence of active mixedfunction oxygenase (MFO) enzymes in vertebrates leads to the metabolism of some xenobiotics such as PAH and therefore the production, accumulation, and/or elimination of oxidized and/or conjugated more polar derivatives (710). These multiple outcomes of exposure make the fate of PAH in finfish more challenging to determine. The present experiment involved exposing male winter flounder (Pseudopleuronectesamericanus), to various concentrations of oil in sediments during 4 months. The exposure conditions, such as the sediment particle size, total organic carbon (TOC), feeding, and metabolism represent an extreme case of bioavailability and bioaccumulation in a northern environment (11). Levels of free hydrocarbons were previously determined in muscle and liver tissues, as were levels of glucuronide and sulfate conjugates in the gall bladder bile (11,121, Concentrations were previously examined in sediments to determine the threshold level above which bioaccumulation or bioelimination was observed. The present study describes the biota-sediment accumulation factors (BSAF = concentration in muscle/ concentration in sediment) observed for specific alkylated naphthalene (NA), phenanthrene (PA),and anthracene (AN) isomers as opposed to the series of C-n alkylated PAH (e.g., for C-lNA, quantify by examining each structural isomer rather than grouping all positions with one methyl substituent). BSAF were examined relative to the structure and known aqueous solubilities of the PAC to gain insight into the mechanism, rate, and equilibria of PAC uptake in muscle of finfish from sediments and to establish a quantitative structure activity relationship (13-16). This relationship is established with the aid of a simple fugacity model of PAC uptake ( 17, 18). The focus is on the level of PAC in muscle. Because this tissue is present in large amount in finfish, it is important from a consumer perspective and is expected to characterize long-term exposure (19). On the other hand, bile metabolites that concentrate in the gall bladder before elimination or recirculation in the hepatic system provide information on previous short-term exposure to contaminants (2023).
Experimental Section The chemical nomenclature used has methyl represented as Me, ethyl as Et, naphthalene as NA, anthracene as AN, phenanthrene as PA, dibenzothiophene as DBT, chrysene as CH, fluoranthene as FL, and pyrene as PY. The following alkylated PAH were quantified in reference to the commercial standards or in reference to reported relative indices. a, 2-MeNA b, 1-MeNA c, 2-EtNA d, 1-EtNA; e, 1,3-diMeNAf, 1,7/1,6-diMeNA;g, 2,3/1,4-diMeNA h, 1,5diMeNA i, 1,2-diMeNA;j, 1,3,7-triMeNA;k,1,3,6-triMeNA; \
VOL. 29, NO. 10, 1995 /ENVIRONMENTAL SCIENCE & TECHNOLOGY 12555
I, 1,4,6/1,3,5/2,3,6-treNA;m. 1.2,7/1,6,7/1.2.6-ueNA; n, 1,4,5/1,2,3-uiMeNAo,3-MePA; p, 2-MePA; q, 2-MeAN; 140 I, 9/4-MePA; s. 1-MeAN; t, 1-MePk Water solubilities were obtained from average reported 120 values in Mackay et al. (24)and Pearlman et al. 123. These 1w valuesareNA,31.8;AN,0.06~PA,1.28;DBT,1.03;FL,0.24: 6 PY, 0.14: CH, 0.003; a, 25.56 b, 25.56 c, 7.96; d, 10.30; e, 280 7.96; h, 3.12; q, 0.03; and t, 0.27 mg/L. Values are also s .= available for the two overlapping g compounds and the s w first of the n isomers, but they were not used because it is 40 not known which of these isomers were present in tissue. Experimental details have been published in Hellou et 20 al. (11). but can be briefly summarized as follows: 16-20 O a b c d e f g h , ) k l m n o P q r S t finfish were exposed to 45 kg of sediments containing 0,5, Alkylated PAH 25,50,1OO,and250mLofHibemiacrudeoil. Thesegroups FIGURE 1. Concentration of specific alkylated PAH in sediments. are referred to as E-0, E-5, E-25, E-50, E-100, and E-250, Letters refer to Structures defined in the Experimental Section. respectively. Exposure lasted from January to April, a time when fish are dormant, naturally not feeding (26). Environmental conditions were as follows: -1 to +3 "C, 30-32 ppt, 300 L seawater; while flounder were mature males, tw 27-29 cm and 243-280 g. The sediment collected before 80 starting the experiment was sampled (pool of three sub$; samples) to determine total organic carbon (TOC = 0.8%), d density (1.6kg/L),and particle size (=-65pm). Lipid content 260 ofmuscle tissue was previouslydetermined onother winter 6% flounder 12-596. mean 3.5%). After an exposure of 4 % s40 months, fish were dissected, and tissues obtained from 10 ;w fish per exposure were analyzed for free PAC and metabo820 lites. E-250 10 w Statisticalanalysis of variance (ANOVA)was performed on the BSAF data obtained on 15 compounds without O a b c d e i g h i ~ k l r n n O p q r S t nondetectable values. Since one sediment sample was Alkylated PAH analyzed from each exposure tank and 10 fish were FIGUREZ. Concentration of specific alkylated PAH in muscle tissue. examined in each tank, thevariability due to the sediment Letters refer to structures defined in the Experimental Section. results is not accounted for. The following equation less substituted ones. It could also be that the variability describes the statistical approach and accounts for 95% of in the more concentrated less alkylated NA derivatives is the observed variability: due to overload of the MFO enzymes. y-.Ilk = gtc.h..f e. Studiesofthechemicdoxidationofsubstituted benzenes t t i kli tjk have indicated that ring degradation increases with increasing degree of alkyl substitution (27). Other studies of where yijr denotes the concentration of the jth compound the metabolic products of n-. sec-, and tert-butylbenzene found in the kth fish exposed to the ith PAH concentration have indicated that oxidation of the ring as opposed to the in sediment. The letters c, f, h, and t represent chemical, branchwill take place when a more highly substituted side fish, interaction, and treatment, respectively. chain is present (28). However, the authors are not aware Results and Discussion of studies on the relative rate of metabolism of a ring or an alkyl substituent of a PAH that would allow conclusions ResultsobtainedfromtheanalysisofspecificalkylatedPAH regarding bioaccumulation. are presented for sediments and muscle tissue (Figures 1 Biota-sediment accumulationfactors representing mean and 2, respectively). Mean concentrations of specific PAH concentration in muscle divided by concentration in in muscle were always more elevated than median consediment (at the end of the exposure) are presented for the centrations (Table 1).reflecting the positive skewness of whole analyzed series ofcomponents, and for the resolved the results. Exposure E-50 showed a larger difference PAC with known solubilities (Figures3 and 4 respectively). between means and medians than the E-100 and E-250 We have previously raised a question regarding the exposures. This difference may reflect a more variable concentration of PAC in the E-250 sediment, since the enzymatic response and hence bioaccumulation at lower normalized fingerprint differed for C-4NA compared to exposure where the MFO enzymes are not all uniformly sedimentsfromE-50andE-100(11). Thisobsenrationdoes induced. It is also possible that the E-50 Esh were less not affect the present results, since no C-4NA are commobile than those in the E-100 and E-250 tanks and mercially available. therefore not uniformly exposed, but this was not visually Three levels of bioaccumulation appear to be present observed. Up to two or three times higher means than (Figure 3). The group with the highest degree of bioacmedians were observed for the smaller and more watercumulation is the monosubstituted naphthalenes (methyl soluble components compared to the largerand somewhat andethyl, a-d) anddimethylnaphthalenes (e-i), while the less soluble alkylated PAH (less than 50% difference). group with the lowest bioaccumulation factors comprises Although present in lower concentration, a certain range C-1 tricyclic PAH lo-t). The trimethylnaphthalenes form of substituted PAH might be metabolized more readilythan
F -
2558. ENVIRONMENTAL SCIENCE &TECHNOLOGY I VOL. 29.
NO. 10. 1995
TABLE 1
Concentration (ng/g, Wet Weight) of Various Alkylated PAH Anlaved in Muscle Tissue muscle d E-50
q r S
t
muscle d E-250
muscle of E-1W
mean
median
SO'
mean
MEDIAN
SO
mean
median
SD
11 5.6 4.9 1.3 1.9 11 5.5 5.4 1.8 2.6 0.52 0.98 4.6 1.8 0.37 0.24 0.24 0.18 0.55 0.16
4.0 3.0 3.5 0.6 1.0 4.0 2.5 2.0 1.o 2.0 0.45 0.50 2.0 0.95 0.35 0.20 0.20 0.15 0.45 0.20
18 9.4 5.3 1.9 2.3 15 7.5 8.0 2.0 2.4 0.30 1.2 5.6 2.4 0.27 0.05 0.03 0.10 0.22 0.05
50 28 8.0 4.7 8.3 46 21 18 7.8 9.0 1.7 2.3 9.4 4.7 0.51 0.86 0.63 0.11 1.3 0.39
11 6.0 2.5 1.0 3.0 9.0 6.0 4.0 2.0 3.0 0.85 1.o 3.0 2.0 0.30 0.55 0.40 0.10 0.80 0.30
122 68 16 11 16 106 43 38 15 17 2.3 3.5 17 7.4 0.55 0.91 0.52 0.04 1.4 0.23
99 74 16 10 27 90 55 45 23 23 5.8 5.5 23 13 1.1 1.1 1.1 0.41 5.1 1.8
64 54 9.5 6.5 16 58 34 29 14 16 4.5 4.0 17 9.0 0.95 0.95 0.95 0.35 4.0 1.5
105 73 10 10 29 86 58 45 23 21 4.8 4.2 17 10 0.80 0.81 0.77 0.25 3.6 1.3
'SD, standard deviation.
FIGURE 3. Biota-sediment accumulation facmn (BSAF). Concentration in musclelconcentration in sediments. There are two scales presentedwheremuscle and sedimemconcentrationsareexpressed in terms of wet weights or [dry weights].
FIGURE 4. Correlation between log BSAF and log water solubility olPAC. LBnenrefertostruchlresdefinedintheExperimentalSection. anintermediareclassofP~1 (j-nl. Tluspoupingcorrelares withexpectedand reponed water solubilities lFigure4; 29, 30). An analysis of variance (ANOVA) indicates an overall decrease in the BSAF going from E-50io E-100.followed by an increase of BSAF in E-250.bur there is considerable variability between PAH. Statistical analysis relies on the experimental results where the variability in muscle results
per treatment is accounted for, while that in sediments (one pool of three subsamples per treatment) is not. The results suggest that to a first approximation BSAF are applicable over this range of concentrations but variability occurs. The log/log relationship between BSAF and water solubility is presented in Figure 4 (for six parental and eight aJkylatedPAC). No obvious consistent dependenceofBSAF on concentration is apparent. It is of interest to compare the BSAF of parental compounds in terms ofsolubilities to that of alkylated PAH. In the present experiment F, PA, DBT, and CH were detected in over 80% of the samples, while FL and PY were present in 50, 80, and 30% of the E-50,E-100, and E-250fish muscle. Other larger PAHs, such as benzlalanthracene (BaA) were not detected. The water solubility of the first three compounds is between 1.83 and 1.03 mg/L, that of CH is the lowest (0.003 mg/L). and that of FL and PY is intermediate (0.242 and 0.145 mg/L; BaA, 0.011 mg/L; 16). Since FL and PY did not accumulate to the extent of CH, it may be that they have a higher tendency to metabolize. This interpretation can besubstantiated, at least for PY, by reponed photochemical data regarding the half-life of tetracyclic compounds that reflects their general reactivity (31, 32). The higher molecular weight of FL and PY and associated surface area could also represent an explanation. Biocnncentrationfacton (BCF)have also been obtained for specific PAH, in Daphnia (33)and in mussels (e.g.. 3436). Values of 2 x 104-4 x lo6 (dry weight of mussels, relative to water) and of 1 x lo2-1 x lo' (wet weight in amphipod, relative to water)were observed in these animals with a neghgible abilityto biotransform PAH. In the present case, it is possible to extrapolate BCF values using the expected concentration of PAH in water rather than the experimental values obtained in sediments. Using eq 3 derived below gives BCF = 0.0051&&4SF The BCF derived from BSAF become for 1-MeNA and 2-MeNA, the more soluble derivatives, 50-450 (dry weight VOL. 29. NO.
10.1995 I ENVIRONMENTAL SCIENCE 8 TECHNOLOGY
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in muscle, relative to water; BCF values would be five times lower in terms of wet muscle weight). For fluorene, with a midrange solubility, the BCF becomes 60-70; while that of chrysene, one of the larger detected PAH, becomes 100220. It has been pointed out byvaranasi et al. (8)andvaranasi and Stein (37)that larger parental PAH (four and five rings) are metabolized more readily than smaller PAH (two and three rings). This statement is partly supported by the ultraviolet fluorescence profile of bile metabolites where the presence of larger species was observed, although in a relatively very low concentration (12). However, in the muscle profile only smaller molecules were detectable (11). Mechanistic Model of PAC Uptake. Although the physical, chemical, and biological phenomena occurring in the exposure system are complex, it is useful to develop and test a relatively simple model describing the uptake process. Presumably an individual PAC desorbs from the sediment into solution in water, while it is taken up by the fish by transfer across gill surfaces as well as by association with food. Some PAC may be degraded or volatilized from the water. Following uptake, there may be metabolic conversion. We model these processes with a simple fugacity model using the concepts explained by Mackay (18).
The concentration of an individual PAC in the sediment C, (mol/m3)results in a fugacity& (Pa) determined by the proportionality constant Z, ([mol.m31/Pa), which depends on the chemical sediment-water partition coefficient, which is controlled by the physical-chemical properties and the organic carbon content. The usual approach is to deduce Z, as Z, = Ko,OCeZw= C,/f,
(1)
where KO,is the organic carbon partition coefficient and is usually40%of&,, the octanol-water partition coefficient (38),OC is the mass fraction of organic carbon (0.0081, is the density of the solid sediment (1.6 kg/L), and& is the Z value of the PAC in water. We assume that the PAC dissolves in water approaching the same fugacity, i.e., fw in water approaches &. The concentration in water approaches .GfW or C, (mol/m3).It follows that if & and f, are equal CJC,
= KO,OC@
(2)
the latter group being a dimensionless partition coefficient. The commonlyused Kp (with units of Llkg) is Ko,OC. Since BCF is CF/CW,and BSAF is CF/CW,where CFis concentration in fish, then
BCF/BSAF = K,,OCe
(3)
Assuming that the fish is exposed to this fugacity v;V or PAC and its internal fugacity @) will approach these values. Biomagnification is likely only if an appreciable fraction of the uptake is in food. Following Clark et al. (13),we can model the uptake from water as follows, using D values as transport and transformation rate parameters.
fs), it will take up
VFZFdfF/dt = DJw - ~F(D,+
(4)
where VF is the fish volume (m3),ZF is the fish Z value (mol/m3Pa),and tis time (h). 0, is the gill uptake D value 2558
ENVIRONMENTAL SCIENCE &TECHNOLOGY / VOL. 29. NO. 10, 1995
and can be estimated as fw&, where G, (m3/h) is the effective volumetric flow rate of water past the gills, Le., including an efficiency term. DM is a metabolism rate D value and can be expressed as VFZF~F where k~ is the firstorder rate constant (h-9 and is 0 . 6 9 3 / ~where ~ / ~ z I i Zh is the metabolic half-life (18). Integrating gives
The concentration in the fish is then CFor ZF~F at any time. This uptake equation is commonly expressed in rate constant form as (39): CF = CW[k1/(k,+ km)l{l - exp[-(k,
+ k,)tI}
(6)
It can be shown that ki is D,/VF&, k2 is D,/VFZF, and k, iS Dm/VFZF (18). This equation suggests that if CFandfF are zero at time zero, then following exposure to a constant f, or G,, the fish fugacity and concentration rise with a characteristic time of VFZF/(D~D,) or a half-time of 0.693v~Z~/(D, + Dm),eventually reaching an equilibrium value for a nonmetabolizing chemical (D, = 01, when fF equals f, or CF equals ZF~,or (ZF/&)C, or BCFC,. The BCF is simply ZF/ G.Usually ZFis estimated as KO,,?,&, where L is the lipid fraction of the fish (3.5%for muscle), thus BCF is also KO,,?,. Since CF approaches LKo,C, and C, approaches C,/ (K,,OQ), it follows that CFwill approach Cs~&,L/Ko~OC~s) or C,BSAF. This group BSAF is a dimensionless biotasediment accumulation factor. Inserting typical values of 0.035 for L, 0.4 KO,for KO,,0.008 for OC, and 1.6 for esgives BSAF as 6.8. If the fish and sediment concentrations are expressed on a weight basis, then we have CFand C,, where CFis c F / @ F and C, is C,/@,and the common BSAF (in units of pg/g dry weight in fish and pglg dry weight in sediment) designated BSAF' is CF/Cs(@s/@F). The important conclusion is that if equilibrium is approached between fish and sediment, using the above data, it is expected that the BSAF will be of the order of 6.8 regardless of KO, since it cancels in the fish and sediment Z values. This has been discussed in greater detail by Parkerton et al. (40),Ankley et al. ( 4 1 ) , DiToro et al. (42), Lake et al. (431, and others. The data in Figure 4 suggest that this near-equilibrium partitioning is occurring to the more soluble compounds for which the BSAF are in the range 0.03-12 for the naphthalenes. It is noteworthythat BSAF are expected and found to be substantially independent of PAC concentration, Le., the points for E-50, E-100, and E-250 overlap. The BSAF values for the larger parental PAH (FL, PY, CH, and higher molecular weight PAH) or less soluble PAC are typically 0.1-0.01 and less, suggesting a failure to approach equilibrium. There are two possible reasons. First, if there is metabolism, the BSAF will be reduced bythefactorD,/(D,+D,) or k2/(k2+km). Itseemsunlikely that there is a systematic increase in the effect of metabolism with decreasing solubility, although it is possible since a slow constant metabolic conversion of all PAC would have a greater effect on the less soluble PAC because they have smaller values of kz or D, is larger compared to 0,. Second, it is possible that uptake is slower for the larger PAC. The time constant for uptake is, as developed earlier, VFZF/(D, + D M )or l/(k2 + k,).
+
It is instructive to insert typical values: VFis about 263 cm3 or 263 x m3, ZF is about 0.035K0,&, and Dw is G w L . Graham (26)determined a respiration rate for winter flounder of 67 L kg-l day-' in the winter. Therefore, for a fish of mass 0.263 kg, G, is 17.6 Llday, i.e., each fish effectivelyremoves PAC from 17.6 L of water each day. We assume k , and D, to be zero, at least initially. The time constant is thus
VFZFIDw= 263 x
0.035Kow/0.04= 0.0023K0, days (7)
The implicationis that to approach equilibriumto the extent of 1 - e-l or 63% will require 0.0023&, days or for naphthalene (log KO, = 3.35; 291, the time will be 5 days. For phenanthrene (log KO, = 4.571, the time is 85 days; for pyrene (logKO,= 5.181,the time is 348 days; and for benzo[alpyrene (log KO, = 6.041, the time is nearly 7 years. As the PAC become more hydrophobic, with a larger KO, and a lower solubility in water, the concentration in water falls and the fish must respire a much larger volume of water to achieve uptake of the ultimate equilibrium value. For a larger PAH, this time can exceed the exposure time and in some cases, even the fish's lifetime. We believe that the basic cause of the low BSAF for the higher PAC is the long time required to reach equilibrium, but it is also possible that there is some metabolism and slower release from the sediments. Note that kl the uptake rate constant is DJ vfz, or G,/Vf or about 67000 day-' for all PAH, thus it is not a slower uptake rate constant that is implied. There is however slower uptake, Le., klc, because c, is lower for the larger PAH. The lower values of c, can be viewed as reduced bioavailability,Le., less PAH in solution and more sorbed to sediments. Crude oils contain volatiles (aromatics with less than 10 carbons), other heterocyclic aromatic compounds, and monocyclic aromatic hydrocarbons with expected higher solubilities than the presently investigated PAC (29, 44). The smaller volatile aromatics with much higher water solubilities are associated with tainting of fish products (forbranching of up to sixcarbons, reported water solubility is above 0.235g/L). We have previously shown that larger monocyclic species, alkylbenzenes, bioaccumulate in tissues and these compounds are more water soluble than larger aromatics (11). More information regarding the biotransformation and half-life of smaller aromatics, including PASH, characteristic of petroleum, their physicalchemical properties, microbial and photochemical degradation, interaction with enzymes, and cell membranes will allow a better understanding of the behavior of petroleum contaminants in various environmental compartments and their modeling to predict bioaccumulation.
Conclusion Flatfish were exposed to several concentrations of a crude oil in sediments. Specific parental and alkylated PAC were determined in muscle and sediments, in order to correlate BSAF with KO,. The bioaccumulation was modeled using a simple fugacity approach and shown to be higher for lower molecular weight PAC in sediments.
Acknowledgments The authors acknowledge the financial support obtained from the Green Plan-Toxic Chemicals Program and from the Program for Energy Research and Development (PERD).
We would also like to thank Dr. W. G. Warren in the Resource Assessment and Survey Methodology Section at the Department of Fisheries and Oceans in St. John's for the statistical analysis of the BSAF results.
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Received for review January 27, 1995. Revised manuscript received May 30, 1995. Accepted June 9, 1995.@ ES9500522
@
Abstract published in Advance ACS Abstracts, August 1, 1995.
