United States Environmental Protection Agency Environmental Research Laboratory Athens GA 30613 Research and Development EPA-600/S3-83-053 Nov. 1983 oEPA Project Summary Fates and Biological Effects of Polycyclic Aromatic Hydrocarbons in Aquatic Systems John P. Giesy, Steven M. Bartell, Peter F. Landrum, Gordon J. Leversee, and John W. Bowling The hypothesis that fates of polycyclic aromatic hydrocarbons (PAH) in eco- systems can be predicted by mech- anistic simulation models based on easily measured properties of the com- pounds in this homologous series was tested. The research involved: 1) de- velopment of a mechanistic, predictive simulation model based on kinetic and thermodynamic considerations; 2) de- velopment of analytical and quality assurance protocols for the extraction and quantification of PAH associated with biological and geological matrices; 3) determination of the vectors of and rate constants for uptake depuration and biotransformation of PAH by aqua- tic organisms and sediments; and 4) comparison of the results of simula- tion and laboratory scale studies to a large scale ecosystem study. Included were studies of the effect of PAH con- centration, temperature, and, other exogenous factors on rate constants and efforts to determine whether rate constants were first order. Laboratory studies indicated that anthracene and benzo(a)pyrene are rapidly biotransformed by fish and dip- teran larvae but not by periphyton com- munities. Biotransformation had a sig- nificant effect on the steady state con- centrations of parent compound and biotransformation products. These re- sults demonstrated that predictions of steady state concentrations based on 14C-labeled parent compound and the octanol-water partitioning coeffi- cient of the parent compou nd wou Id be in error. Thus, the octanol-water par- titioning coefficient would not be a good predictor of the behavior of PAH in aquatic organisms. Uptake and de- puration rate constants were first order for fish but not dipteran larvae. Induc- tion of biotransformation and changes in biotransformation rate over time means that predictions of long-term disposition in the ecosystem from short term pharmacokinetic studies, using radio-labeled compounds, will be mis- leading for compounds that are bio- transformed. Anthracene (approximately 12 jog/l) was acutely toxic to bluegill sunfish dosed in outdoor channel microcosms. This mortality was not observed in laboratory studies and was shown to be caused by a photo-mediated toxic mechanism. Therefore, laboratory tox- icity studies on PAH must be con- ducted under the same lighting con- ditions if the results of these studies are to be realistic representations of field conditions. The modeled processes that most influence PAH transport included loss- es to volatilization, photolytic degra- dation, sorption to suspended particu- late matter and sediments and net uptake by biota. The biota in the model included phytoplankton, periphyton, rooted macrophytes, bacteria, zoo- plankton, two functionally defined benthic invertebrate components and two functionally defined categories of ------- fish. Model simulations were com- pared to results of experiments con- ducted in artificial streams. A 0.06 u. molar solution of anthracene in ethanol was continuously added into the head- waters for 15 days. The model accu- rately predicted the dissolved anthra- cene concentration through time and space. Uptake by periphyton was over- estimated by the model; however, the rate of depuration of anthracene by periphyton was reasonably simulated. Photolytic degradation appeared to be the most important pathway of flux with the channels, both experimentally and in the simulations. This Project Summary was developed by EPA's Environmental Research Lab- oratory, Athens, GA, to announce key findings of the research project that is fully documented in a separate report of the same title (see Project Report ordering information at back). Introduction Polycyclic(polynuclear) aromatic hydro- carbons (PAH or PNA) are a homologous series of compounds composed of two or more condensed benzene rings with oc- casional incorporations of cyclopentene rings, such as in the fluorenes, or"hetero- atoms" (N, 0 or S). PAH are derived from natural and man-made sources and are widely distributed in the environment PAH occur as natural products from plants and microbes and from natural pyrolytic processes such as forest fires and volcanic activities. Man-made sources include in- dustrial processes but the major source is combustion of fuels. Most of the PAH in the environment are due to human activi- ties and freshwater and nearshore marine environments are enriched with PAH. More than 230,000 metric tons of PAH enter the oceans and surface waters each year. The toxic, mutagenic and carcinogenic properties of PAH have been much studied Many PAH are carcinogens or procarcin- ogens in animals and maa Part of the hazard assessment process is to deter- mine the exposure of animals and man. This required an understanding of the fate and transport processes in an ecosystem. Because of their ability to bioconcentrate lipophylic compounds such as PAH, aqua- tic organisms are an important vector to man. Also, because of their flowing, sol- vating character and organic sediments, surface waters serve as both a transport mechanism and a sink for PAH. Because of the vast differences be- tween simple laboratory tests and com- plex field situations, scientists have formed conceptual and operational bridges be- tween the two systems. These include mechanistic simulation models and micro- cosms, which are operational models or simplifications of environments. In this study, both of these types of models were employed to investigate the fate and trans- port of PAH in aquatic systems. Summary This program of study tested the overall hypothesis that a dynamic, mechanistic simulation model of the fate of PAH in an aquatic system can be constructed, based on characteristics of the compound of interest and the environment to which it is released. The study tested the ability to predict the fate of anthracene introduced into a channel microcosm using a simu- lation model, which had been param- eterized independently. In addition, the simulation model was used to guide the laboratory investigations. By using a syn- thesis of microcosm, modeling and labor- atory studies, the authors were able to guide their research to answer some of the most pertinent questions related to an understanding of the dynamics of anthra- cene in aquatic systems. The fate of aromatics model (FOAM) predicts the concentrations of PAH in water, sediment phytoplankton, periphy- ton, macrophytes, zooplankton, two ben- thic invertebrate components, bacteria, suspended paniculate matter and herbiv- orous and carnivorous fish. The overall simulation model is organized as a main program (MAIN) (Fig. 1), which calls sub- routines that calculate solar radiation (SOLAR), movement of water (HYDRO), solubility of PAH, and resuspension and settling of suspended components and graphs the absolute and relative concen- trations of PAH in each compartment (Table 1). Other submodels calculate pho- tolysis (PHOTO), volatilization (VOL) and sorption to sediments (SORP). The model is a mass balance, generalized reach model (Fig. 2). The biological components are simulated as a generalized production model with the PAH inputs partitioned into the biotic components (Fig. 3). All of the simulated processes in FOAM are cor- rected for temperature effects. FOAM, which is programmed in FORTRAN, re- quires a small number of input variables (relative to many dynamic, mechanistic simulation models) and is easy to use. Modular Program Structure Inputs Fates of Aromatics Model (FOAM) Figure 1. Schematic representation of modular subroutine structure of FOAM. ------- Each subroutine calculates part of the overall derivative for change in biomass or PAH mass in each state variable. FOAM simulates the dynamics of biological pro- duction and PAH dynamics through space and time. Each state variable value is printed in matrix form where row elements are values at a specific time for each reach. Column elements are temporal values in a particular reach. A complete listing of Table 1. Output from FOAM. Each Variable is Simulated Hourly Parameter Irradiance Allochthanous organic matter External PAH loading Periphyton biomass Macrophyte biomass Benthic invertebrate biomass Clam Biomass Bacterial biomass Fish biomass Suspended particulate organics Dissolved organics Bottom sediments Suspended inorganic particulates Settled detritus PAH in periphyton PAH in macrophytes PAH in benthic insects PAH in bacteria PAH in fish predaceous herbivorous Suspended organic particulates PAH in dissolved organic matter PAH in bottom sediments PAH in suspended inorganic particulates PAH in settled detritus PAH dissolved in water PAH which has been transferred Units langleys-h'1 g • dry weight • m "2 gPAH-m* g- m"2 g- m'2 g- m'2 g- m'2 g- m'2 g- m'2 g- m'2 g- m'2 g- m'2 g- m'2 g- m'2 fi mol PAH- g ' ', dry weight H mol PAH- g'1, dry weight p. mol PAH- g ' ', dry weight p. mol PAH- g ' ', dry weight [I mol PAH- g'1,dry weight fj. mol PAH- g'1,dry weight /A mol PAH- g~',dry weight H mol PAH- g ' ', dry weight /i mol PAH- g ' 1, dry weight p. mol PAH- g'1,dry weight fi mol PAH- g ' ', dry weight H mol PAH- T1 nmolPAH-r' General Reach Model Segmented Stream REACH, Figure 2. Conceptualization of generalized stream reach transport model. FOAM is available from the authors. It should be noted that model development is a dynamic process and FOAM has been undergoing continuous development since it was initially programmed FOAM was parameterized to simulate anthracene dynamics in the channel micro- cosms facility located at the Department of Energy's (DOE) Savannah River Plant (SRP). The channel microcosms facility is a pass-through system consisting of six separate cinder-block-lined channels each 91.5 m long, 0.61 m wide, and 0.31 m deep. Located at the upper end of each channel is a pool 3.1 m long, 1.5 m wide and 0.9 m deep. At the lower end of the facility is a single large pool 10.2 m long, 3.1m wide and 1.0 m deep. For these studies, the channels and headpools were lined with a 0.05 cm thick black polyvinyl chloride film and the bottom covered with 0.05 m of washed quartz sand. Water was pumped from a deep well and treated so that the inorganic water quality was similar to that of surface waters in the upper coastal plain. Water flows were monitored by V-notch wiers on each headpool. Flow rates of 75.7 l/min were maintained by input valves. This resulted in a current velocity of 1.0 x 10 "2 m/sec and a retention time of 2.5 h. The water depth in the channels was main- tained at 20 cm. The channels were natu- rally colonized with algae, bacteria, fungi and aquatic invertebrates. Clams and fish were held in the channels in cages for the validation study. Laboratory studies demonstrated that benzo(a) pyrene (BaP) and anthracene were rapidly biotransformed by bluegill sunfish and chironomid larvae but not unionid clams or periphyton assemblages. Bio- transformation rates were dependent on temperature and time of exposure. The rates of biotransformation also influenced the bioconcentration factors predicted from short-term pharmacokinetic studies. Temperature and food ration also influ- enced the rates of uptake and depuration. Uptake and depuration were adequately described by first-order relationships. Depuration was generally multiphasic with some biotransformation products bound to tissues, such that they were very slowly depurated. Recovery of anthracene from sediments was inversely proportional to the time of exposure. Internal standards, added at the time of extraction, did not allow accurate determination of extraction efficiencies. Drying of sediments resulted in reduced recovery from sediments A benzene-aceto- nitrile (1:2; V/V) extract resulted in the best recovery of anthracene from sedi- ------- Simulation of PAH Flux Through Streams f "--~J Benthic \ J Invertebrates REACH^ REACH, REACH* Figure 3. Schematic representation of FOAM model. merits. Capillary gas-liquid chromatogra- phy coupled to mass spectrometry (GC- MS) showed that anthracene could be extracted from sediments and separated from naturally occurring organic com- pounds but anthraquinone (a transforma- tion product of anthracene) could not, Dissolved organic carbon (humic sub- stances) interfered with the extraction of anthracene and BaP from water by macro- reticular resins. Humic acids also reduced the availability of anthracene, benzo(a)py- rene and dimethylbenzanthracene to D. magna but increased the availability of 3- methylcholanthrene and dibenzanthracena The presence of suspended particulates also reduced the availability of PAH to D. magna. FOAM accurately simulated and pre- dicted the flux along physical-chemical pathways (Table 2). The model, however, was less accurate in predicting the ac- cumulation and biotransformation of PAH by aquatic biota. Future versions of pre- dictive simulation models should be kinet- ically based, as FOAM is, if accurate in- formation on cycling is to be predicted. This type of model, however, requires a great amount of information. Because of the scale of the input parameters, models such as FOAM will be useful in describing overall processes and fluxes along dif- ferent pathways but will not be very useful in simulating the concentrations of PAH and PAH transformation products in in- dividual biotic components. Also, some of the physical processes, which are impor- tant in determining the fates of PAH in natural systems, are discontinuous func- tions or catastrophic events, such as storms, which do not lend themselves to mathematical simulations. Therefore, mod- els of the type developed here will always be limited to relatively gross predictions Accurate prediction of concentrations in individual types of organisms may not be attainable. The channel microcosms were useful for testing the reliability of FOAM to sim- ulate the behavior of PAH in a complex ecosystem. The greatest utility of the channel microcosms, however, was in allowing studies to be conducted under more natural conditions than allowed by laboratory systems. From these studies we learned that exposure to sunlight caused acute mortality due to anthracene. Thus, laboratory studies of anthracene Table 2. Predicted and Observed Concentrations of Dissolved Anthracene in Channels Microcosms Time Dawn observed predicted Reach 1 (Head) 0.066 0.056 mol anthracene "' Reach 3 (Middle) 0.065 0.056 Reach 5 (Tail) 0.063 0.055 Noon observed predicted 0.067 0.056 0.045 0.045 0.028 0.036 toxicity to aquatic organisms do not ac- curately predict toxicity observed under more natural conditions. Although micro- cosms may not be used as a screening tool for individual compounds, they are useful in studies of classes of compounds and to verify laboratory and simulation conclu- sions. Because of their scale, however, microcosms will never by useful in valida- tion of long-term or global simulation models. The test of the benchmark hy- pothesis was only partly supported by our studies. Future simulations will need to consider more complex measures of chemical be- havior. The proposed use of octanol/water partitioning coefficients shows promise for predicting uptake by organisms but not biotransformation. Thus, the benchmark approach will probably not give adequate predictions of the dynamics of organic compounds in complex environments. A coordinated synthesis of information on ecosystem structure and function is required to assess environmental impacts of any technology that must ultimately be interfaced with the environment While this research was on PAH compounds (anthracene and benzo(a)pyrene specifi- cally) it supports the hypothesis that valid generalizations about the behavior of gen- eral classes of organic compounds in com- plex environments can be made from knowledge about the compounds obtained in relatively simple laboratory studies and the environments to which these com- pounds are released. Knowledge of this type can be transferred to other organic compounds and has broad applicability. Recommendations Future studies of the fates and effects of trace contaminants should be conducted in laboratory, field, and simulation modes concurrently. All three modes of investi- gation added to the overall understanding of the dynamics of PAH in aquatic eco- systems. Simulation models should be developed to predict general behavior of PAH in aquatic systems. That is, to determine when the greatest mass of PAH accumu- lates and where the most sensitive eco- system components are. Where physical and chemical processes dominate, simu- lation models will be able to accurately predict the overall dynamics of PAH, but rare events of large magnitude will reduce the accuracy of predictions on a short- term basis. Optimization of time step duration relative to system level variability needs to be further investigated to in- crease the accuracy of predictive models. ------- The current state of predictive simu- lation models will not allow the accurate prediction of concentrations of single PAH in individual species but can be useful in simulating overall processes in a gross manner. Future simulation should be kinetic in nature but the relationships used to predict rate constants need to be based on structure-activity relationships. The channel microcosms used in this study were sufficient to test some simu- lation processes, and the authors recom- mend the use of this type of a system in future studies. Microcosms of this type, however, will not be useful as screening tools. The utility of the realism of such systems was demonstrated by the photo- mediated toxicity of anthracene effect ob- served in the microcosm, which was not observed under laboratory conditions. This type of system needs to be used to validate processes that are indicated by laboratory and/or simulations because they allow testing in a more complex and more natural system than that of the laboratory, while not releasing trace con- taminants to the biosphere J. P. Giesy is with Michigan State University, East Lansing, Ml 48824; S. M. Bartell is with Oak Ridge National Laboratory, Oak Ridge, TN; P. F. Landrum is with the National Oceanographic and Atmospheric Administration, Ann Arbor, Ml 48104; G. J. Leversee is with Keene State College, Keene. NH03431, andJ. W. Bowling is with the University of Georgia, Savannah River Ecology Laboratory, Aiken, SC 29801. H. W. Holm is the EPA Project Officer (see below). The complete report, entitled "Fates and Biological Effects of Polycyclic Aromatic Hydrocarbons in Aquatic Systems," (Order No. PB 83-250 191; Cost: $20.50, subject to change} will be available only from: National Technical Information Service 5285 Port Royal Road Springfield, VA 22161 Telephone: 703-487-4650 The EPA Project Officer can be contacted at: Environmental Research Laboratory U.S. Environmental Protection Agency College Station Road Athens, GA 30613 •&U. S. GOVERNMENT PRINTING OFFICE: 1983/759-102/0795 ------- United States Environmental Protection Agency Center for Environmental Research Information Cincinnati OH 45268 BULK RAT U.S. POSTA PAID Cincinnati, C Permit No. G Official Business Penalty for Private Use $300 ------- |