Sorption of polychlorinated biphenyls (PCB) to clay particulates and effects of desorption on phytoplankton

Water Res. Vol. 17. No. 4. pp. 383-387, 1983 Printed in Great Britain.All rights reserved

0043-1354/83/040383-05503.00/0 Copyright © 1983PergamonPress Ltd

SORPTION OF POLYCHLORINATED BIPHENYLS (PCB) TO CLAY PARTICULATES AND EFFECTS OF DESORPTION ON PHYTOPLANKTON GLYNIS M. NAu-RITTERand CHARLESF. WURSTER Marine Sciences Research Center, State University of New York, Stony Brook, NY 11794, U.S.A. (Received December 1981)

Abstract--The sorption of polychlorinated biphenyls (PCB) on illite and chlorite, two minerals of defined composition, was investigated. Illite particles adsorbed higher [~4C]PCB (Aroclor 1254) concentrations than did chlorite particles, with equilibrium concentration factors between particles and water being 1.4 x 104 for illite and 1.0 x 10" for chlorite. Desorbed PCB inhibited photosynthesis and reduced chlorophyll-a content of natural phytoplankton assemblages within dialysis membrane bags suspended in the water of a tidal marsh. There was no significant difference in effects on the phytoplankton of PCB desorbed from the two minerals. The rate of [~4C]PCB desorption was dependent on the initial concentration on the clay particles. The rate of [~4C]PCB loss from bags with particles was slower than that from bags without particles.

INTRODUCTION

The occurrence and biological effects of polychlorinated biphenyts (PCB) in the environment have been extensively studied in recent years (Hutzinger et al., 1974; National Academy of Sciences, 1979). The physical and chemical properties of PCB cause their removal from water by sorption onto surfaces including particulate matter (Karickhoff et al., 1979). PCB concentrations on particulates were related to the organic content and size of the particles (Choi & Chen, 1976; Wildish et al., 1980; Nau-Ritter et al., 1982a) and to the aqueous solubility of the chemicals (Haque et al., 1974; Haque & Schmedding, 1975). Recent studies suggest that equilibrium partitioning describes the sorption of PCB to particles from water and explains the temporal and spatial distribution of PCB in the environment (Dexter & Pavlou, 1978; Pavlou & Dexter, 1979). Since smaller particles contain larger surface areas, suspended finer particulate matter in the environment may accumulate relatively large quantities of PCB (Steen et al., 1978; Hiraizumi et al., 1979). Particle-sorbed PCB in the environment may be deposited within bottom sediments (Schlesinger, 1979) or transported in suspension to other areas. Suspended particles may provide prolonged and increased exposure of the biota to PCB. Because of their relatively high lipid solubility, PCB in water are readily accumulated by organisms (Tulp & Hutzinger, 1978) including fish, which thereby become a human health hazard. PCB transferred from sediments may accumulate in phytoplankton (Powers et al., 1982), where detrimenContribution 315 of the Marine Sciences Research Center, State University of New York at Stony Brook. 383

tal effects on primary production may occur (Harding & Phillips, 1978; Nau-Ritter et al., 1982b). Most particle-PCB sorption studies have involved natural sediments (Hiraizumi et al., 1979; Karickhoff et al., 1979; Steen et al., 1978). This paper compares the sorption of [t4C]PCB onto illite and chlorite clays, two minerals of defined composition and the subquent in situ desorption in a tidal salt marsh. The effects on natural phytoplankton communities of PCB desorbed from both minerals are also presented. Illite and chlorite were chosen because they are the dominant minerals in the clay fraction of the Hudson River sediments (McCrone, 1967). The Hudson is the most PCB-polluted U.S. waterway, with large quantities of PCB occurring in sediments north of Albany, New York (Boppet al., 1981). MATERIALS A N D M E T H O D S

Laboratory

IUite and chlorite were suspended in filtered (Millipore, 0.22#m) sea-water. Since chlorite is a denser clay than illite, suspensions were prepared for equal dry weights of the particles (450mg illite or chlorite l-1) and for equal particle numbers (450mg illite l-1 and 2000 mg chlorite l- x). Particle suspensions were sized and counted by a Particle Data ElectroZone Celloscope interfaced with a PDP8/M computer (Digital Equipment Corp., Maynard, MA). [t4CJPCB (Aroclor 1254, 31.3 #Ci mmol-1, lot 872-193, New England Nuclear Corp., Boston, MA) in 10#1 of methanol was injected into 10-ml illite or chlorite suspensions in 50-ml centrifuge tubes, yielding a final PCB concentration of 1/~gml- 1 (Nau-Ritter et al., 1982a). The particle suspensions were continuously agitated on a shaker table. External standards measured the sample counting efficiencies during liquid scintillation counting. This method

3x4

(}I~xls M N~t-REiII:~ ~md CHARI.I:S [:. Wti
was preferable to the use of internal standards by NauRitter t,t al. (1982a1. which underestimated the quenching caused by the clay particles in the fluor. Spccilic surface areas of the illite attd chlorite particles were measured on a Quantasorb Sorption System (Quantachrome Corp, Greenvale. NYI.

[a)

8.4 F "[llite ( 4 5 0 mg I -t) - - - Chlorite ( 4 5 0 rng I -t) .... Chlorite { 2 0 0 0 mg I -r)

0

Fieht

Desorption of [~+C]PCB from illite and chlorite occurred in dialysis membrane bags under natural conditions in Flax Pond (Powers et aL, 1976, 19771, a tidal salt marsh on the north shore of Long Island. New York (Woodwell et al., 1977). 100#g [~+C]PCBg ~ was sorbed onto illite (450 mg t i) and chlorite (450 and 20t)0 mg 1- ~1 particles, which were pelleted by centrifugation and further suspended in 0.22-/~m filtered sea-water within dialysis bags. Equal weights of illite and chlorite (72 mgl 1} and equivalent particle numbers (72 mg illitel ~ and 320 mg chlorite l -~) were suspended in triplicate in nine dialysis bags, yielding PCB concentrations of 7.2, 7.2 and 32/~g 1 ~, respectively. At a concentration of 10#g of PCBI -] [~+C]PCB was also injected directly into two other bags containing 0.22-/~m filtered sea-water. Collection of 40-ml samples from each of three bags within each of three clay suspensions permitted determination of the amount of [~+C]PCB in the water and on the particles at 0, 24, 48 and 72 h. Similar 40-mt samples were collected from each bag where [~+C]PCB was injected directly into the water. The dialysis membranes were measured for radioactivity on the last day, when they contained 0.03% of the PCB concentration initially added to the bags. [~+C]PCB activity associated with the particles, water, dialysis membranes and methanol washes of the sampling containers was measured by liquid scintillation counting. The effects on natural phytoplankton communities of PCB (non-radiolabeled Aroclor 1254, Monsanto Co., St Louis, MO) sorbed onto equal weights (450 mg 1- ]) of illite and chlorite were measured for 4 days in Flax Pond. Photosynthetic t+C-fixation and chlorophyll-a content were measured by the techniques of Nau-Ritter et ul. (1982b). PCB II00ygg ~ of clay dry wtl was added daily at a suspended solids concentration of 72 mg I 1 to natural phytoplankton assemblages contained in dialysis bags. Phytoplankton communities in the presence and absence of daily additions of uncontaminated illite and chlorite served as control communities. Statistical handling of the data, including analyses of variance IANOVAsl and regression statistics, followed Sokal & Rohlf 11969L

RESULTS AND D I S C U S S I O N

Laboratory experiment

Most of the illite and chlorite particles were less than 1 6 # m equivalent spherical diameters (ESD) (Fig. la). Structural differences between the two minerals were evident when particle volumes were electronically determined. Chlorite particles had larger ESDs than did iltite particles, the modal ESDs being 25 and 5/+m, respectively (Fig. lb). The larger chlorite therefore contained fewer particles in a 450 mg 1 - ' suspension than did illite at the same concentration. Total particle volumes, however, were similar for the 450 mg 1-~ suspensions of both minerals (Table 11. Adsorption of [~+C]PCB to particles was rapid during the first 3 h. When [ t + C ] P C B was added to the 450-mg 1-~ mineral suspensions, equilibrium between the [~+C]PCB on the particles and that in the water

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P a r t i c l e d i a m e t e r (/~m) Fig. 1. Particle concentration-size distribution of illite 1450mgl -~1 and chlorite 1450 and 2000mg1-11 suspensions. The upper graph (a) is the number of particles at each equivalent spherical diameter (ESD}, whereas (b) represents the total volume of particles at each ESD. was reached more rapidly with the smaller illite than with the larger chlorite particles (Table iI. Several P C B adsorption studies utilized Freundlich adsorption isotherms, which assume a constant surface area at equilibrium (Harding & Phillips, 1978: Hiraizumi et al.. 19791. This assumption is not always valid in natural systems, however. We therefore employed the concentration factor (K) equation derived by Dexter & Pavlou (19781, where K represents the weight of PCB associated with particles divided by that in the water (Table II. PCB concentration on illite and chlorite particles was plotted against that in the water at each sampling time (Fig. 2). The slopes of the lines differed {P < 0.01) according to an F-test comparison between regression coefficients (Sokal & Rohlf. 19691. Itlite initially had a greater surface area a n d capacity for P C B adsorption than did chlorite, but particles disintegrated within the centrifuge tubes as the experiment progressed, thereby increasing particle surface .area. Concentration factors for illite a n d chlorite are not

385

PCB sorption to particles and effects on phytoplankton Table 1. Particle volumes, surface areas and concentration factors (K) for illite and chlorite Time (h) Illite (450 mg I- 1) 1 3 6 9 Chlorite (450 mg 1- 1) l 3 6 12

Particle volumes (ppm)*

Specific surface areal

Equilibrium concentration factor:~ ( × 10 3)

63.4

19.9

0.62 14.79 12.40 12.00

63.3

2.1

0.84 6.57 8.98 10.15

*Particle volumes (electronically determined) expressed as 10 6 pm 3 ml -~ or ppm of suspended volume. fSpecific surface area of the particles expressed as m 2 g - 1 as determined before initiating the experiment. ++Concentration factors, K, calculated from K = Cx (particles)/Cx (water), where Cx (particles) is gg of PCB kg- 1 of clay and Cx (water) is #g of PCB 1-1 of water (Dexter & Pavlou, 1978; Pavlou & Dexter, 1979). directly related to their indicated surface areas because the finest particles resulting from particle breakdown were not recovered quantitatively. Other authors found PCB sorption to be directly proportional to particle surface area (Hiraizumi 1979; Karickhoff et al., 1979). Illite and chlorite represent 75~o of the clay fraction of Hudson River sediments, where they exist in a ratio of 3:2, respectively (McCrone, 1967). Chlorite contains a brucite layer Mg3(OH)6 , which increases the spacing between consecutive layers from 10 A in illite to 14.2 A in chlorite (Hurlburt & Klein, 1977; Riley & Chester, 1971). Both minerals are non-expanding clays with similar chemical, physical and crystallographic properties (Hurlburt & Klein, 1977). Field experiment

When [14C]PCB-contaminated illite and chlorite particles were suspended in situ for 3 days, the greatest desorption to the water occurred within the first 24 h (Fig. 3). Since different initial [14C]PCB concen-

trations occurred on the particles, three significantly (P < 0.05) different lines described the concentrationdependent rates of desorption to the water. Lines were drawn from least squares fitting of logarithmically transformed data for easy comparison of desorption rates. By normalizing the [~4C]PCB concentrations to the initial amounts on the particles (Fig. 4), no significant difference was found among the desorption rates from illite and chlorite at either suspended solids concentration after a posteriori testing for differences among regression coefficients by the simultaneous test procedure (Sokal & Rohlf, 1969). The presence of clay particles increased the residence time of PCB within the dialysis bags. [~4C]PCB concentrations were higher in bags with clay particles than in bags with particle-free water (Fig. 4). A significant (P < 0.01) linear relationship described the loss of PCB from bags with particle-free water following a logarithmic transformation of time. Estimates of PCB concentrations to which phytoplankton were exposed at various times during earlier toxicity studies in Flax Pond (Nau-Ritter et al., 200

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Ceq (ng I"l) Fig. 2. PCB particle/water relationships for illite and chlorite. Each point represents a mean of three samples of the concentration of PCB on the particles (log X/M) and in the water (log C=q) taken at 1, 3, 6, (9 or 12) h.

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Fig. 3. [=4C]PCB remaining on illite (450mg1-1) and chlorite (450 and 2000 mg 1- ~) during a 72-h desorption to water within dialysis bags suspended in Flax Pond. Each point is a mean of three values with sampling times at 0, 24, 48 and 72 h.

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Decreased photosynthesis due to PCB-sorbed particulates was previously observed by Nau-Ritter et aL. (1982b) using different natural phytoplankton communities. The effects on phytoplankton from the daily additions of 100 ~g of PCB g- 1 (dry wt) at suspended solids concentrations of 72 mg 1- 1 were not statistically different between iltite- and chlorite-treated assemblages. Reduced 14C-fixation and chlorophyll-a content probably occurred on Day 3 in illite-treated communities because of decreased light available for photosynthesis from increased turbidity. Greater turbidity from suspended illite resulted from the greater number of illite particles, as compared with the number of chlorite particles, in the 72 mgl ~ ~ daily additions.

+Illite (450 mgl -I) = • Chlorite (450 mg I- ) i ~ o Chlorite ( 2000 mg I- ) •~ i o r t i c l e - f r e e water

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Log [(tirne +l)h] Fig. 4. [t*C]PCB sorbed onto illite (450mgl ~) and chlorite (450 and 2000 mg 1- t) or remaining in particle-free water. [~*C]PCB is expressed as % of initial PCB concentration within the dialysis bags during a 72-h desorption to water in Flax Pond. Each point is a mean of three percentages at sampling times of 0, 24, 48 and 72 h.

CONCLUSION

Illite sorbed more [14C]PCB from water and reached equilibrium more rapidly than did chlorite, the concentration factors from water to particles being 1.4 × 104 and 1.0 × 104, respectively. The rates of desorption of [L*C]PCB from equal weights, or equal numbers, of illite and chlorite particles to natural waters were similar, as were the toxic effects on natural phytoplankton of PCB desorbed from the two minerals. If illite and chlorite are minerals typically involved in the sorption of PCB to sediments, then desorption of PCB from suspended sediments

1982b; O'Connors et al., 1978; Powers et al., 1976, 1977) can now be made from these data. A similar decline in [14C]PCB concentration in the bags was observed in earlier Flax Pond studies (Biggs et al., 1980). When PCB-contaminated illite and chlorite particles were suspended with natural phytoplankton in Flax Pond, a significant (P < 0.05) decrease from the control communities in photosynthetic 14C-assimilation and chlorophyll-a content was observed (Fig. 5). I0,000

A

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/<:

1000

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I

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Days Fig. 5. [t*C]uptake (a) and chlorophy!l-a content (b) of naturalphytoptankton communities exposed to PCB sorbed onto illite and chlorite particles at a concentration of l00 #g of PCB g- t of clay. Itlite and chlorite were added daily to the phytoptankton communities at a concentration of 72 m g l - 1. *Indicates PCB was sorbed onto the clay particles.

PCB sorption to particles and effects on phytoplankton appears to be insensitive to dissimilarities between particles. Acknowledoements--The authors thank R. George Rowland for technical assistance. This work was supported by grants from the New York State Department of Environmental Conservation, the MESA New York Bight Project (National Oceanic and Atmospheric Administration) and the New York Sea Grant Institute.

REFERENCES Biggs D. C., Powers C. D., Rowland R. G., O'Connors H. B. & Wurster C. F. (1980) Uptake of polychlorinated biphenyls by natural phytoplankton assemblages: Field and laboratory determination of 1-14C]PCB particlewater index of sorption Envir. Pollut. (Ser. A) 22, 101-110. Bopp R. F., Simpson H. J., Olsen C. R. & Kostyk N. (1981) Polychlorinated biphenyls in sediments of the tidal Hudson River, New York. Envir. Sci. TechnoL 15, 210-216. Choi W. W. & Chen K. Y. (1976) Association of chlorinated hydrocarbons with fine particles and humic substances in near-shore surficial sediments. Envir. Sci. TechnoL 10, 782-786. Dexter R. N. & Pavlou S. P. (1978) Distribution of stable organic molecules in the marine environment: Physical chemical aspects. Chlorinated hydrocarbons. Mar. Chem. 7, 67-84. Haque R. & Schmedding D. W. (1975) A method of measuring the water solubility of hydrophobic chemicals: Solubility of five polychlorinated biphenyls. Bull. envir, contain. Toxic. 14, 13-18. Haque R., Schmedding D. W. & Freed V. H. (1974) Aqueous solubility adsorption and vapor behavior of polychlorinated biphenyl Aroclor 1254. Envir. Sci. Technol. 8, 139-142. Harding L. W, Jr & Phillips J. H. Jr (1978) Polychlorinated biphenyls: Transfer from microparticulates to marine phytoplankton and the effects on photosynthesis. Science 202, 1189-1192. Hiraizumi Y., Takahashi M. & Nishimura H. (1979) Adsorption of polychlorinated biphenyl onto sea bed sediment, marine plankton and other adsorbing agents. Envir. Sci. Technol. 13, 580-584. Hurlburt C. S, Jr & Klein C. (1977) Manual of Mineralogy (after James D. Dana), 19th Edition, 532 pp. Wiley, New York. Hutzinger O., Safe S. & Zitko V. (1974) The Chemistry of PCB, 269 pp. CRC Press, Cleveland, OH. Karickhoff S. W., Brown D. C. & Scott T. A. (1979) Sorption of hydrophobic pollutants on natural sediments. Water Res. 13, 241-248. McCrone A. W. (1967) The Hudson River Estuary: sedi-

w.R. 1 7 / ~ c

387

mentary and geochemical properties between Kingston and Haverstraw, New York. J. sedim. Petrol. 37, 475-486. National Academy of Sciences (1979) Polychlorinated Biphenyls, 182 pp. NAS Publication, Washington, D.C. Nau-Ritter G. M., Wurster C. F. & Rowland R. G. (1982a) Partitioning of [I'4C]PCB between water and particulates with various organic contents. Water Res. 16, 1615-1618. Nau-Ritter G. M., Wurster C. F. & Rowland R. G. (1982b) Polychlorinated biphenyls (PCB) desorbed from clay particles inhibit photosynthesis of natural phytoplankton communities. Envir. Pollut. (Ser. A)28, 177-182. O'Connors H. B. Jr, Wurster C. F., Powers C. D., Biggs D. C. & Rowland R. G. (1978) Polychlorinated biphenyls may alter marine trophic pathways by reducing phytoplankton size and production. Science 201,737-739. Pavlou S. P. & Dexter R. N. (1979) Distribution of polychlorinated biphenyls (PCBs) in estuarine ecosystems. Testing the concept of equilibrium partitioning in the marine environment. Envir. Sci. Technol. 13, 65-71. Powers C. D., Rowland R. G. & Wurster C. F. (1976) Dialysis membrane chambers as a device for evaluating impacts of pollutants on plankton under natural conditions. Water Res. 10, 991-994. Powers C. D., Rowland R. G., O'Connors H. B. Jr & Wurster C. F. (1977) Response to polychlorinated biphenyls of marine phytoplankton isolates cultured under natural conditions. Appl. envir. Microbiol. 34, 760-764. Powers C. D., Nau-Ritter G. M., Rowland R. G. & Wurster C. F. (1982) Field and laboratory studies of the toxicity to phytoplankton of polychlorinated biphenyls (PCBs) desorbed from fine clays and natural suspended particulates. J. Great Lakes. Res. 8, 350-357. Riley J. P. & Chester R. (1971) Introduction to Marine Chemistry, 465 pp. Academic Press, New York. Schlesinger R. B. (1979) Natural removal mechanisms for chemical pollutants in the environment. BioScience 29, 95-101. Sokal R. R. & Rohlf F. J. (1969) Biometry, 776 pp. Freeman, San Francisco. CA. Steen W. C., Paris D. F. & Baughman G. L. (1978) Partitioning of selected polychlorinated biphenyls to natural sediments Water Res. 12, 655-657. Tulp M. T. M. & Hutzinger O. (1978) Some thoughts on aqueous solubilities and partition coefficients of PCB and the mathematical correlation between bioaccumulation and physicochemical properties. Chemosphere 7, 849-860. Wildish D. J., Metcalfe C. D., Akagi H. M. & McLeese D. C. (1980) Flux of Aroclor 1254 between estuarine sediments and water. Bull. envir, contam. Toxic. 24, 20-26. Woodwell G. M., Whitney D. E., Hall C. A. S. & Houghton R. A. (1977) The Flax Pond ecosystem study: exchanges of carbon in water between a salt marsh and Long Island Sound. Limnol. Oceanogr. 22, 833-838.