Monocyclic Aromatic Hydrocarbons in the Ocean

CHAPTER 14

Monocyclic Aromatic Hydrocarbons in the Ocean 14.1 M O N O C Y C L I C AROMATIC H Y D R O C A R B O N S IN S E A W A T E R

14.1.1 Sources of Monocyclic Aromatic Hydrocarbons in the Ocean A large number of monocyclic aromatic hydrocarbons, benzene and its alkyl homologues, is present in crude and refined petroleum products (Neff et al., 1994). Some also are natural products, synthesized by many bacteria, fungi, plants, and possibly animals (Fishbein, 1984). Some crude oils contain several percent monocyclic aromatic hydrocarbons (Table 79). Automotive gasoline, a low-boiling distillate of crude oil, typically contains 12 to more than 50 percent total monocyclic aromatic hydrocarbons (Cline et al., 1991; King, 1992); toluene usually is most abundant (Table 80). Total U.S. demand for crude oil in 1995 was 2.23 x 109 L/d, of which 1.24 x 109 L/d was for gasoline (Beck, 1996). Thus, the amounts of monocyclic aromatic hydrocarbons produced and consumed are large. U.S. production of benzene alone was estimated to be 2.4 billion metric tons in 1982 (Fishbein, 1984). The monoaromatic hydrocarbons of greatest concern in the environment are benzene, toluene, ethylbenzene, and m-, p-, and o-xylenes (BTEX) (Figure 9). BTEX are low molecular weight monoaromatic hydrocarbons that are moderately soluble in fresh water and seawater and are highly volatile (Table 81). Solubility in seawater is lower than that in fresh water because of salting out (solubility of nonpolar organic chemicals decreases as the concentrations of dissolved inorganic salts increase). BTEX have log KowS from 2.13 to 3.20, indicating a moderate affinity for partitioning into tissue lipids of aquatic organisms and sorption to sediment organic matter. Because of their chemical/physical properties, BTEX are not persistent in seawater, bind only weakly to marine sediments, and are not bioaccumulated to high concentrations by marine organisms. The log KowS of the BTEX compounds are all lower than 3.5; therefore, according to EPA (1991), they have a low potential to bioaccumulate. Trimethyl benzenes and more highly alkylated

225

226 Bioaccumulation in Marine Organisms monoaromatic hydrocarbons have much lower aqueous solubilities, higher log KowS and lower volatilities than BTEX (Table 81) and, therefore, behave differently than BTEX in the environment. BTEX reaches the marine environment in domestic and industrial waste water effluents (including treated produced water from production platforms: Tables 1 and 9), runoff from land, and spills of crude and refined petroleum products. Other sources may be important locally. For example, two-stroke and four-stroke outboard engines inject large amounts of BTEX directly into the water in which they are operated (Jfittner, 1994). Jiittner (1994) reported that during 10 minutes of operation, a medium-sized outboard motor burning unleaded gasoline injects 107 mg of benzene, 258 mg of toluene, 22 mg of ethylbenzene, and 108 mg of xylenes into the once-through cooling water.

Table 79. Concentrations of several monocyclic aromatic hydrocarbons (MAH) in three crude oils from the Northwest Shelf of Australia. Concentrations are mg/kg (ppm). From Neff et al. (1998a). Chemical Benzene Toluene Ethylbenzene m-Xylene p-Xylene o-Xylene Isopropylbenzene n-Propylbenzene 1-Methyl-3-ethylbenzene 1-Methyl-4-ethylbenzene 1-Methyl-2-ethylbenzene 1,3,5-Trimethylbenzene 1,2,4/ 1,2,3-Trimethylbenzene sec-Butylbenzene 1-Methyl-3-isopropylbenzene 1-Methyl-4-isopropylbenzene 1-Methyl-2-isopropylbenzene 1-Methyl-3-n-propylbenzene 1-Methyl-4-n-propylbenzene 1,3,dimethyl-5-ethylbenzene 1,2-Diethylbenzene 1.3-Diethylbenzene 1,4-Diethylbenzene 1-Methyl-2-n-propylbenzene 1,4-Dimethyl-2-ethylbenzene 1,2-Dimethyl-4-ethylbenzene 1,3-Dimethyl-2-ethylbenzene 1,3-Dimethyl-4-ethylbenzene 1,2-Dimethyl-3-ethylbenzene 1,2,4,5-Tetramethylbenzene 1,2,3,5-Tetramethylbenzene 1,2,3,4-Tetramethylben zene Total MAH ND Not detected.

Condensate 6750 28,514 4506 24,982 8694 8612 828.9 1439 5944 1991 1609 5792 10,426 302.2 715.0 409.9 139.1 1475 562.5 1737 238 ND ND 497 806 1149 144 904 386 530 819 348 121,247

Light Crude 2566 26,520 6356 33,987 10,071 12,413 1167 2410 8536 2953 2530 7843 14,240 462 298 682 215 2477 1016 2519 ND ND ND 866 1201 1818 232 1384 596 763 1214 630 147,966

Medium Crude 3259 5915 1487 8312 3011 3218 327 695 3161 1056 946 3292 6541 193 475 315 86 1198 476 1465 ND ND ND 390 688 1045 155 828 355 611 869 406 50,774

Chapter 1 4 - Monocyclic Aromatic Hydrocarbons in the Ocean 227

Table 80. Concentration range of monocyclic aromatic hydrocarbons and naphthalene in 31 gasoline samples from Florida. Concentrations are weight percent. From Cline et al. (1991).

Chemical Benzene Toluene Ethylbenzene o-Xylene m-,p-Xylenes

Concentration Range

Chemical

0.7 - 3.8 4.5 - 21 0 . 7 - 2.8 1.1 - 3.7 3.7 - 14.5

Propylbenzene Methylethylbenzenes Trimethylbenzenes Naphthalene

Concentration Range 0.13 1.5 0.6 0.2

-

0.85 3.2 1.1 0.5

Table 81. Physical/chemical properties of benzene, toluene, ethylbenzene, xylenes, and a typical trimethylbenzene. Data from Eastcott et al. (1988) and Abernethy et al. (1986).

Compound

Molecular Weight

Seawater Solubility (mg/L)

Benzene 78.1 1,398 Toluene 92.1 389 Ethylbenzene 106.2 114 p-Xylene 106.2 114 m-Xylene 106.2 108 o-Xylene 106.2 133 1,2,4-Trimethyl120.2 41 Benzene * Equivalent to M/m 3 in air divided by M/m 3 in water.

Benzene

Log Kow

Henry's Law Constant (H)*

2.13 2.65 3.13 3.18 3.20 3.13 3.58

0.224 0.244 0.404 227 0.294 0.176 0.253

Toluene

o-

p-

m-

Ethylbenzene

o-, m-, p-xylene (dimethylbenzene)

Figure 9. Chemical structuresof the monocyclicaromatic hydrocarbons,benzene,toluene, ethylbenzene, and xylenes (BTEX).These aromatic hydrocarbonsusually are abundant in petroleum and producedwater.

228 Bioaccumulation in Marine Organisms Gasoline-powered vehicles may emit up to 38 mg toluene and 11 mg ethylbenzene in exhaust per kilometer driven; diesel-powered vehicles emit BTEX at a lower rate (Hampton et al., 1983). Air at gasoline stations may contain 0.06 to 180 ppm benzene (Foo, 1991). Indoor air in homes may contain 10 to 40 ktg/m3 benzene and 15 to 17 ktg/m3 toluene, derived from smoking, and evaporation from paints, wallboard, etc. (Bauhamra, 1995). Concentrations of benzene in urban air frequently are in the range of 4 ktg/m3 to occasionally as high as 114 ktg/m3 (Wathne, 1983). The mean concentration of benzene in the atmosphere of 10 Canadian cities in 1988 and 1990 was 4.4 ktg/m 3, with a range of 1.2 to 14.6 ktg/m3 (Hughes et al., 1994). The background concentration of benzene in the air of southern Ontario is about 1.9 ktg/m3 (McLeod and Mackay, 1999). The air of U.S. and Canadian cities contains 3 ktg/m 3 to more than 800 ktg/m3 toluene (Greenberg, 1997). However, BTEX concentrations in rain water usually are low. Kawamura and Kaplan (1983) reported a concentration of 0.096 ktg/L total BTEX (minus benzene) in a rain sample collected in Los Angeles, CA. Much higher concentrations of BTEX may be encountered in the air for a short time (a few days) after a major oil spill or oil fire (Hanna and Drivas, 1993; Bouhamra, 1995). Hanna and Drivas (1993) modeled the time/concentration patterns of BTEX and several saturated hydrocarbons in the air over the oil spilled in the Exxon Valdez oil spill in Prince William Sound, AK (Table 82). Concentrations of BTEX reached highest concentrations in the air over the spreading slick within the first three hours after the spill. Highest concentrations in the air ranged from 0.65 parts per million, volumetric (ppmv) for o-xylene to 8.24 ppmv for toluene. Concentrations of C 6 to C 9 alkanes ranged from 1 to 4.4 ppmv. Mass emissions of toluene to the atmosphere from the spilled oil increased rapidly after the spill, reaching a maximum in excess of 20,000 kg/hour between 8 and 10 hours after the spill. The maximum evaporation rate of benzene was about 10,000 kg/hour nine hours after the spill. The relatively low concentrations of volatile hydrocarbons in the air, despite the high mass emission rates shortly after the spill can be explained by the large surface area of the rapidly-spreading slick. 14.1.2 Concentrations of Monocyclic Aromatic Hydrocarbons in Seawater Although the amounts entering the marine environment undoubtedly are very large, concentrations of BTEX in seawater and estuarine waters generally are very low (Table 83). Concentrations of individual BTEX compounds usually range from 0.001 ktg/L to about 0.2 ktg/L, except near point sources of BTEX, such as domestic sewage treatment plant outfalls, refinery outfalls, produced water discharges, and oil spills. For example, BTEX concentrations in the Narragansett Bay system are highest in the Providence River near wastewater outfalls; concentrations decrease sharply with distance down the bay, and concentrations are quite low in Rhode Island Sound off the mouth of the bay (Wakeham et al., 1982). In the Gulf of Mexico, BTEX concentrations are higher in nearshore waters than offshore. The concentration of total C3-benzenes in Mississippi River water near Memphis, Tennessee, is 0.092 ktg/L but is below the method detection just south of New Orleans (DeLeon et al., 1986). Before produced water discharges to shallow coastal waters were prohibited, nearbottom waters in shallow canals and bayous in coastal Louisiana receiving large-volume produced water discharges sometimes contained up to 10 ktg/L of individual BTEX compounds (Rabalais et al., 1991). Concentrations of individual and total BTEX compounds

Chapter 1 4 - Monocyclic Aromatic Hydrocarbons in the Ocean 2 2 9 Table 82. Maximum estimated hourly-average concentrations of several volatile aromatic hydrocarbons in the air over the crude oil slick from the Exxon Valdez oil spill in Prince William Sound, Alaska. From Hanna and Drivas (1993).

Compound

Hour After Spill of Highest Concentration

Concentration (ppmv)

1 1 2 3 3

4.86 8.24 0.83 0.65 2.00

Benzene Toluene Ethylbenzene o-Xylene m- & p - X y l e n e s

Table 83. Concentrations of benzene, toluene, ethylbenzene, and total xylenes in river and marine waters. Concentrations are in/~g/L.

Location

Benzene

Toluene

Providence R., RI Narragansett B a y , RI Rhode Island Sound Vinyard Sound, MA B r a z o s R., TX Gulf of Mexico Coastal Gulf of Mexico Coastal LA near PW Discharges Near Well Blowout off Texas Near Ixtoc-I

0.053 - 1.14

0.05 - 7.90

0 . 0 1 9 - 0.11

0.016 0.044 0.005 0.18 0.01 - 0.05

Blowout, Mexico Gas Vent, Gulf of Mexico

0.002 - 0.16 --0 . 0 0 4 - 0.23 0 . 0 0 9 - 0.10 0.006 0.175 < 0 . 0 4 - 57

0.013 0.048 0.004-

17.6

Ethylb-enzene 0.004-

3.40

0.001 - 0.021 <0.001 0.011 0.002 - 0.022

Xylenes

Reference

0.011 - 13.4

W a k e h a m et al., 1982 W a k e h a m et al., 1982 W a k e h a m et al., 1982

0.013 0.041 <0.001 0.08 0 . 0 0 6 - 0.09

0.005 0.11 0.004 0.376 0.01 - 0.06

0.0004 0.004 0.001 - 0.015

0.0020.056 0.003 0.034 0.01 - 0.035

< 0 . 0 4 - 32

< 0 . 0 4 - 0.91

< 0 . 0 4 - 17

0.003 . 0.029 0.003-

0.004 - 0.05

.

.

.

0.002-

1.00

0.68

0.07

Sauer, 1 9 8 1 a R a b a l a i s et al., 1991

0.011 0.051

B r o o k s et al., 1978

0 . 0 1 6 - 22.6

B r o o k s et al., 1981

7.60 0.43

G s c h w e n d et al., 1982 M c D o n a l d et al., 1988 Sauer, 198 l a

0.33

Sauer, 1981b

230 Bioaccumulation in Marine Organ&ms decreased sharply with distance from the discharges. In more open coastal environments, BTEX concentrations rarely exceeded 0.1/2g/L. BTEX compounds in produced water discharges to well-mixed open ocean waters are diluted rapidly. Twenty meters down-current from a production platform discharging 11 million L/d of produced water containing an average of 6,410 pg/L total BTEX to the Bass Strait off southeast Australia, the average concentration of BTEX is 0.43/~g/L, a dilution of 14,900-fold (Terrens and Tait, 1996). The most abundant monoaromatic hydrocarbons in both the produced water and ambient seawater are toluene and xylenes. BTEX concentrations may be elevated in the water column under oil slicks from oil spills or well blowouts. Total BTEX concentrations under the spreading slick from the Ixtoc-I blowout in the Bay of Campeche, Mexico, approached 100/~g/L (Brooks et al., 1981). The blowout released large volumes of crude oil at the sea floor; the oil rose slowly through the water column to the sea surface, allowing large amounts of soluble hydrocarbons to partition into the water. BTEX concentrations in the upper water column of spill-path areas of Prince William Sound, Alaska, in the months after the Exxon Valdez oil spill were nearly always below 10 ktg/L (Neff, 1990). Background concentrations of BTEX compounds in seawater are very low and reflect an equilibrium between concentrations in surface waters and in the overlying air (Sauer, 1980). The concentration of total xylenes in a seawater sample from a reef off Bermuda is 0.00014 ktg/L (Ehrhardt and Bums, 1990). The concentrations of benzene and toluene in a seawater sample from 1,000 m in the Caribbean Sea are 0.0016 and 0.0015 ktg/L, respectively (Sauer, 1980). Concentrations of benzene, toluene, ethylbenzene, and o-xylene in seawater in equilibrium with 1 part per billion (volumetric) of total volatile light hydrocarbons in the overlying air are 0.027, 0.021, 0.018, and 0.019 ktg/L, respectively (Sauer, 1980). The most likely reason for the low concentrations of BTEX in seawater, even in the locations such as the northwestem Gulf of Mexico where inputs from produced water apparently are quite large, is that removal of BTEX from the water is rapid (Kennicutt et al., 1988). The main removal mechanisms for BTEX from the water column are: a) airsea exchange (evaporation); b) adsorption to particles and sedimentation; c) biodegradation; and d) photolysis. BTEX because of their volatility, evaporate rapidly from water. Evaporation is quantitatively the most important route of loss of BTEX from water. Gschwend et al. (1982) estimated that under moderately calm conditions when BTEX concentrations in the water are much higher than those in the overlying atmosphere, the residence time of BTEX in the aqueous phase is approximately two days. Under more turbulent conditions with good vertical mixing, half-lives for BTEX in the water column may be as low as a few hours (Brooks et al., 1984). Half-lives of BTEX compounds in marine mesocosms are in the range of a few days to a few weeks, depending on temperature (Wakeham et al., 1983, 1985, 1986). The equilibrium distribution of toluene among the water, sediment, and air in a model aquatic ecosystem is approximately 0.9%, 0.4%, and 98.6%, respectively. Dewulf et al. (1998) reported average concentrations of individual monocyclic aromatic hydrocarbons in surface water from the southern North Sea ranging from 15.2 ng/L (benzene) to 46.6 ng/L (m- and p-xylenes). Average concentrations in the overlying atmosphere ranged from 413 parts per trillion volumetric (benzene) to 854 pptv for mand p-xylenes. Surface waters served as a source of BTEX to the overlying atmosphere,

Chapter 1 4 - Monocyclic Aromatic Hydrocarbons in the Ocean 231

with average flux rates ranging from 0.8 ktg/m2/day for o-xylene to 9.5 ktg/m2/day for mand p-xylenes. The mean flux rates of benzene and toluene from surface water to the atmosphere were about 4 ktg/mZ/day. 14.2 M O N O C Y C L I C AROMATIC HYDROCARBONS MARINE SEDIMENTS

IN

Sorption to and deposition with suspended sediments usually is not a quantitatively important mechanism for removal of BTEX from the water column. There is no relationship in the Brazos River, Texas, between concentrations of suspended particulate matter and BTEX concentrations in the water (Brooks et al., 1984). Before termination of the discharges, concentrations of monocyclic aromatic hydrocarbons were low in sediments near discharges of produced water to shallow-water channels in Louisiana salt marshes (Table 84). The Delacroix Island facility discharged an average of 314,000 L/day of produced water at the time that discharges were terminated (DOE, 1997b). The salinity of the produced water was about 135 %0. The Four Isle Dome facility discharged an average of about 608,000 L/day of produced water shortly before termination of discharges. The water had a salinity of 152 %o, about 30 times the salinity of the brackish receiving waters. Because of the high salinity of the produced water from the two discharges, it sank upon discharge, increasing contact between produced water chemicals and sediments below the discharge. BTEX concentrations in sediments under the two discharges were 0.58/tg/g dry wt and 0.24/tg/g (Table 84). Sediments at Four Isle Dome also contained 0.19 ktg/g C3-benzenes and 0.15/tg/g C4-benzenes. Higher molecular weight monocyclic aromatic hydrocarbons were enriched in sediments more than low molecular weight compounds, reflecting the greater hydrophobicity of the former. At three produced water discharge sites monitored by Armstrong et al. (1979) and Neff et al. (1989), concentrations of individual BTEX compounds in the produced water discharges were in the range of <10 to 6,370/tg~. Sediments near two of the discharge sites did not contain detectable concentrations of BTEX. At the Trinity Bay facility, concentrations of benzene, toluene, and ethylbenzene in the ambient water just down-current

Table 84. Concentrations of monocyclic aromatic hydrocarbons in produced water and sediments near shallow-water (1 - 2 m) discharges of produced water to salt marshes in southern Louisiana. Concentrations are in pg/L (water) and pg/kg dry wt (sediment). From Dept. of Energy (1997b).

Compound

Delacroix Island Prod. Water Sediments Benzene 230 91 Toluene 610 ND Ethylbenzene 41 69 Xylenes 410 420 Total BTEX 1291 580 C3-Benzenes NA NA C4-Benzenes NA NA ND Not detected. NA Not analyzed.

Four Isle Dome Prod. Water Sediments 2,700 13 1,600 45 100 19 750 163 5,150 240 200 190 36 152

232 Bioaccumulation in Marine Organisms from the produced water discharge were 1.5, 3.2, and 3.1/tg/L, respectively. Most BTEX concentrations in the underlying sediments were below the method detection limit. Small amounts of toluene and ethylbenzene, but no benzene, were retained in some sediments. Less BTEX was retained in sediments than would be predicted by their log KocS, which are approximately 2.0. This may result from rapid biodegradation by sediment microbes. There is very little information about the concentrations of BTEX in marine sediments. As shown in Table 84 and discussed above, small amounts of monocyclic aromatic hydrocarbons may accumulate in sediments near produced water discharges to shallow, poorly mixed estuarine waters (Armstrong et al., 1979; Neff et al., 1989; DOE, 1997b). Wakeham et al. (1985, 1986) reported that although some toluene does adsorb to suspended particles in mesocosms, there is no accumulation of BTEX in bottom sediments. Ten percent of the toluene added to mesocosms in winter and 5 percent of the toluene added to mesocosms in summer adsorbs to suspended particles. Surficial sediments near the waste water outfall for the Palos Verdes sewage treatment plant, California, contains 0.5 ng/g dry wt ethylbenzene and less than 1 ng/g benzene and toluene, even though the effluent contains 14,220, and 210/tg/L, respectively, of these compounds (Gossett et al., 1983). 14.3 D E G R A D A T I O N HYDROCARBONS

OF MONOCYCLIC

AROMATIC

IN WATER AND SEDIMENTS

Microbial degradation of BTEX, although relatively rapid in the water column and surficial sediments under both aerobic and anaerobic conditions (Chiang et al., 1989; Ball and Reinhard, 1996), is slower than volatilization when the water temperature is low. Benzene is completely degraded in one day in a mesocosm simulating conditions in oxygenated ground water (Dyreborg et al., 1998). Biodegradation probably is not a quantitatively important mechanism for removing BTEX from the water column or surface sediments. Stromgren et al. (1995) measured the biodegradation rate of produced water chemicals in the laboratory. BTEX and volatile organic acids degrade most rapidly, followed by phenols and low molecular weight PAHs. In most cases, more than half the BTEX is lost in 28 days at 20~ Wakeham et al. (1985) reported that in marine mesocosms, biodegradation is the most important mechanism for removal of toluene from the water column during the summer. Under winter conditions, biodegradation is slow and evaporation is the main mechanism for removal of toluene from the water. Under aerobic conditions, monocyclic aromatic hydrocarbons in water and sediments are degraded rapidly (Morgan et al., 1993; Atlas, 1995). However, degradation rates are much slower than evaporation rates, so biodegradation usually is not quantitatively important in removing monocyclic aromatic hydrocarbons from the water column and surface sediments. Degradation of monocyclic aromatic hydrocarbons in anoxic sediments is slow and incomplete (Alvarez and Vogel, 1995; Atlas, 1995; Langenhoff et al., 1996). Toluene and xylenes, but not benzene and ethylbenzene, are biodegraded slowly by anaerobic bacteria in anoxic sediments. The main products of anaerobic toluene degradation are benzoic acid, benzyl alcohol, and benzaldehyde (Edwards et al., 1994) Photooxidation of BTEX in water may contribute to the disappearance of these compounds from the water column. Photooxidation products of alkylbenzenes have been detected at concentrations seven to ten times higher than the concentrations of parent compounds in surface waters of Bermuda and the Arabian Gulf (Ehrhardt and Douabul,

Chapter 14 - Monocyclic Aromatic Hydrocarbons in the Ocean 233

1989; Ehrhardt and Bums, 1990). These observations indicate that photooxidation of BTEX and other alkylbenzenes is rapid and represents an important mechanism for removal of these compounds from the water column. Photooxidation products of BTEX also are abundant in marine air (Harvey, 1995). The main degradation products of photooxidation of monocyclic aromatic hydrocarbons in smog are unsaturated anhydrides, such as 2,5-furandione, 3-methyl-2,5-furandione, and 3-ethyl-2,5-furandione (Forstner et al., 1997). 14.4 B I O A C C U M U L A T I O N

OF MONOCYCLIC

AROMATIC

H Y D R O C A R B O N S BY M A R I N E O R G A N I S M S BTEX compounds have moderate aqueous solubilities and high lipid solubilities. Therefore, they bioaccumulate rapidly in the lipid-rich tissues of marine organisms. BTEX are nonpolar (un-ionizable) organic compounds. Therefore, they should partition between the ambient water and tissue lipids of marine organisms in direct relation to their hydrophobicities and lipophilicities, which are proportional to their log KowS. If this is the case, the regression equation of Veith and Kosian (1983) (equation 3 above) or other similar regressions (Neff and Bums, 1996) should provide a reasonable estimate of the wet-weight BCF for each BTEX compound. In addition, most nonpolar organic compounds do not possess a specific mode of toxicity. Instead they induce toxic responses when they accumulate to a critical concentration in tissue (particularly membrane) lipids, causing nonspecific narcosis (Abernethy et al., 1988). McCarty et al. (1992) evaluated the relationship between acute toxicity to aquatic organisms and physical/chemical properties of a large number of nonpolar organic chemicals whose mode of toxicity is thought to be through nonspecific narcosis. They developed a regression equation, based on data for 150 chemicals, relating the median lethal concentrations (LC50) of nonpolar organic chemicals, such as BTEX and PAHs, to their log Kows: Log LC50 (mM)= -0.90Log Kow + 1.71

(9)

The equations of Veith and Kosian (1983) and McCarty et al. (1992) can be used to predict the BCF and acute toxicity of BTEX compounds to marine organisms (Table 85). The estimated BCFs for BTEX compounds range from 19 for benzene to 134 for mxylene. These BCFs, for the most part, are considerably higher than measured BCFs for BTEX compounds in marine and freshwater organisms. The microalga Selenastrum capricornutum rapidly bioaccumulates all the BTEX compounds when exposed to an aqueous solution containing 50,000/tg/L total BTEX (approximately equal concentrations of each compound) (Herman et al., 1991). Equilibrium between the water and algal cells is reached within 30 minutes. BCFs at apparent equilibrium range from 42.7 for benzene to 257 for m-xylene. These BCFs are approximately two times higher than those estimated by the Veith and Kosian (1983) equation. The authors showed that the BTEX compounds are absorbed into the cells of the algae and not merely adsorbed to the cell wall, so passive adsorption can not explain the higher than expected bioaccumulation. The algae release accumulated BTEX when returned to hydrocarbon-free culture medium. Depuration is nearly complete within 30 minutes.

234 Bioaccumulationin Marine Organisms Table 85. Bioconcentration factors (BCF), estimated by the regression equation of Veith and Kosian (1983), and median lethal concentrations (LC50), estimated by the regression equation of McCarty et al. (1992) for BTEX compounds in marine organisms.

Compound Benzene Toluene Ethylbenzene p-Xylene m-Xylene o-Xylene

Log Kow 2.13 2.65 3.13 3.18 3.20 3.13

Estimated BCF 19 49 118 129 134 118

Estimated LCs0 (~tg/L) 48,000 19.000 8,300 7,500 7,200 8,300

Manila clams Tapes semidecussata accumulate up to 4.24/tg/g wet wt (~ 21/zg/g dry wt) total BTEX during exposure for four days to a water-soluble fraction of Cook Inlet crude oil containing approximately 3,500 ~g/L total BTEX (Nunes and Benville, 1979). Benzene and p-xylene are not detected in the clam tissues (detection limits, 0.6 and 0.1/tg/g, respectively). Toluene accumulates to the highest concentration, 2.2/tg/g wet wt at four days. The clams rapidly release the aromatic hydrocarbons when returned to hydrocarbon-free seawater. Marine rotifers Brachionus plicatilis accumulate ~4Cbenzene rapidly from water to concentrations up to 1,000 times the concentration in the exposure water (Echeverria, 1980). The rotifers metabolize the benzene to more polar phenols that are retained in the rotifer tissues after the rotifers are returned to clean seawater, possibly accounting for the high apparent BCF. Atlantic salmon Salmo salar accumulate BTEX compounds in muscle tissue during short-term exposure to the water-soluble fraction of Flotta North Sea crude oil (Heras et al., 1992). Toluene is accumulated to the highest concentration (up to 12/tg/g wet wt) followed by m- + p-xylenes (~ 5/tg/g) during exposure to a water soluble fraction containing 1,540/tg/L total hydrocarbons (mostly BTEX). Coho salmon Oncorhynchus kisutch and starry flounder Platichthys stellatus accumulate C2-benzenes (ethylbenzene and xylenes) during exposure for up to six weeks to the water-soluble fraction of Prudhoe Bay crude oil (Roubal et al., 1978). The flounder accumulate more alkylbenzenes than the salmon do. Highest concentrations in muscle tissue are 0.66/zg/g dry wt and 5.5/tg/g in salmon and flounder, respectively, representing BCFs of 2.4 and 20, respectively. C2benzenes are accumulated to similar concentrations in liver and gills of the flounder. Both fish release the alkylbenzenes rapidly when returned to clean seawater. Herring Clupea harengus pallasi eggs and larvae accumulate benzene during short-term exposures to the hydrocarbon in water and food. BCFs are about 10 in embryos and yolk sac fry after about 12 hours of exposure. Following exposure for 48 hours to 2,100/tg/L benzene in seawater, fed and unfed herring larvae contain wholebody residues of 6.22/zg/g wet wt and 2.78/tg/g benzene, suggesting that some benzene is accumulated from food. However, bluegills Lepomis macrochirus are unable to bioaccumulate toluene from their food (Berry and Fisher, 1979). When dolly varden Salvelinus malma in seawater are force-fed 14C-toluene, they accumulate the most radioisotope in muscle (Thomas and Rice, 1986). Toluene is not absorbed efficiently from the gut of the fish. Seawater-acclimated dolly varden accumulate toluene to higher

Chapter 14- Monocyclic Aromatic Hydrocarbons in the Ocean 235 concentrations than freshwater-acclimated fish do; the difference may be due to more rapid metabolism and excretion of toluene in the freshwater fish. Herring Clupea harengus pallasi accumulate 14C-benzene and 14C-toluene in several soft tissues during exposure for up to two days to 100/tg/L of each of these aromatic hydrocarbons in seawater (Korn et al., 1977). Highest concentrations are in intestine and pyloric caeca, suggesting that absorption of monoaromatic hydrocarbons through the gut is low. Gills also contain relatively high concentrations of benzene and toluene (0.73 and 1.0/tg/g wet wt, respectively), suggesting that gills are the main route of uptake. Concentrations are higher in organ tissues than in muscle, in agreement with the distribution of lipids in the tissues. The highest concentration of radioactivity is found in the gall bladder of the fish; however, nearly all the radioactivity in the gall bladder is associated with metabolites of benzene and toluene. More BTEX (except benzene) accumulates in ovaries than in muscle of adult, spawning herring during exposure to the water-soluble fraction of Cook Inlet crude oil (Rice et al., 1987). Benzene cannot be quantified in the fish tissues by the methods used. The BCF for toluene in mature ovaries and in muscle tissue are 49 and 16, respectively. BCFs for ethylbenzene, and the three xylenes in ovary and muscle are 112 to 118 and 29 to 33, respectively. The BCFs for ovaries are very close to the estimated values (Table 85). The lower BCFs in muscle probably are due to a lower lipid concentration in this tissue, compared to ovaries, especially during the late stages of ovarian maturation. Similar results are obtained in northern anchovys Engraulis mordax and striped bass Morone saxatilis (Korn et al., 1976). Metabolites of C3-benzenes accumulate rapidly in winter flounder Pseudopleuronectes (Pleuronectes) americanus during exposure of the fish to sediments containing Hibernia crude oil (Hellou and Upshall, 1995), indicating that alkyl benzenes are readily oxidized, conjugated, and excreted via the bile in marine fish.

14.5 CONCENTRATIONS OF M O N O C Y C L I C AROMATIC H Y D R O C A R B O N S IN TISSUES OF MARINE ORGANISMS Most laboratory studies of BTEX bioaccumulation use high, environmentally unrealistic exposure concentrations. The test organisms bioaccumulate the BTEX compounds rapidly, but also release them rapidly, often during continued exposure to the compounds in solution (Struhsaker, 1977). Bioaccumulation of BTEX from food (food chain transfer) appears to be inefficient (Whipple et al., 1981). Therefore, one would not expect to encounter high concentrations of BTEX compounds in tissues of marine animals collected from natural marine environments. However, there are very few published values for the concentrations of BTEX in the tissues of marine organisms. Whelan et al. (1982) analyzed low molecular weight aromatic compounds in tissues of four species of macroalgae grown in large culture tanks at Woods Hole Oceanographic Institution. Two species, Ulva latuca and Hypnea musciformis, each contain 0.020/tg/g dry wt of benzene. The other two species, Gracilaria tikvahiae and Ascophyllum nodosum, do not contain detectable concentrations of benzene. No other monocyclic aromatic hydrocarbons were sought. It is uncertain if the two algae accumulate benzene from the water or biosynthesize it. Several others of the C 1 through C 8 organic compounds detected in the algae definitely are products of biosynthesis. Benzene, toluene, and ethylbenzene were analyzed in the tissues of several species of benthic and demersal marine invertebrates and fish from the vicinity of the outfall for the

236 Bioaccumulation in Marine Organisms Palos Verdes sewage treatment plant in the Southem Califomia Bight (Gossett et al., 1983). Benzene is present at low concentrations in the livers of three species of fish and one composite invertebrate sample (Table 86). Toluene and ethylbenzene are present in the liver of two species of fish. Only dover sole Microstomus pacificus and white croaker Genyonemus lineatus contain quantifiable residues of all three monoaromatics in liver. Concentrations of these BTEX compounds are very low compared to concentrations of total BTEX reported in liver and gonadal tissues of striped bass Morone saxatilis from the Carquinez Straits area of the San Francisco Bay-Delta, Califomia (Whipple, 1979). Not all fish contain detectable levels of BTEX. Among those that do, concentrations in livers of females and males range from 0.10 to 16.4/tg/g dry wt and 0.10 to 28.7/tg/g, respectively. Gonadal tissues of those female and male bass containing detectable concentrations of BTEX, contain 0.10 to 6.6/tg/g and 0.10 to 8.4/tg/g, respectively. The reason for the higher concentrations of BTEX in male than in female tissues is unclear, but may be related to differences in lipid concentrations in liver and gonadal tissues of males and females. In January 1993, the oil tanker Braer ran aground off Shetland, Great Britain, and spilled 84,000 tons of a partly biodegraded North Sea crude oil (Glegg and Rowland, 1996). Because of the high dispersibility of the oil and the severe weather conditions at the time of the spill, much of the oil was dispersed into the water column. Shortly after the spill, razor shells Ensis spp. that washed up at several locations along the shore were collected and their soft tissues were analyzed for several aromatic hydrocarbons characteristic of the spilled oil. The bivalves contained 0.48 to 0.85/tg/g dry wt toluene and 0.33 to 0.47/zg/g ethylbenzene in their soft tissues. The bivalves contained higher concentrations of naphthalene and methylnaphthalenes and phenanthrene and methylphenanthrene than monocyclic aromatic hydrocarbons. It is uncertain if the bivalves became contaminated with petroleum aromatic hydrocarbons before or after washing up on the shore.

Table 86. Concentrations of benzene, toluene, and ethylbenzene in sewage effluent, sediments, and tissues of demersal/benthic marine animals near the outfall for the Palos Verdes sewage treatment plant, California. Concentrations are/Jg/L (effluent) and ng/g dry wt (sediments and tissues). From Gossett et al. (1983). , ,

Sample

Benzene

Toluene

Ethylbenzene

Effluent Sediments Pacific Sanddab Citharichthys xanthostigma Liver Scorpionfish Scorpaena guttata Liver Dover Sole Microstomus pacificus Liver Croaker Genyonemus lineatus Liver Shrimp Sicyonia ingentis Whole Invertebrates

220 <1 <5

210 <1 <5

14 0.5 <0.3

80 260

<5 5

<1.5 1.5

75 <5 40

125 <5 <10

20 <1.5 <1.5

Chapter 14- MonocyclicAromatic Hydrocarbons in the Ocean 237

14.6 TOXICITY OF MONOCYCLIC AROMATIC HYDROCARBONS TO MARINE ORGANISMS Predicted median lethal concentrations of BTEX compounds range from 48,000 ktg/L for benzene to 7,200/~g/L for m-xylene (Table 85). These values are in reasonable agreement with the empirical toxicity data in the U.S. EPA AQUIRE database (Table 87). The empirical toxicity values, except that for benzene, are higher than the estimated LCs0s. Much of the data used to develop the regression ofMcCarty et al. (1992) were for Daphnia and other small, freshwater crustaceans that are more sensitive than most other aquatic species to monocyclic aromatic hydrocarbons (Abemethy et al., 1998). Marine crustaceans and fish have a similar sensitivity to BTEX compounds (Neff, 1979). Toxicity does increase (LCs0 decreases) in all species as molecular weight of the BTEX compound increases. The differences in toxicity of the four C2-benzene isomers and the two trimethylbenzenes probably are related to effects of the positions of alkyl groups on the molar volume of the compounds, which in tum affect the critical body burdens in the organism (Abemethy et al., 1986, 1988). The concentrations of BTEX compounds required to reduce growth of the microalga Selenastrum capricornutum by 50 percent range from 41,000 ktg/L for benzene to 4,000 to 5,000 ktg/L for ethylbenzene and the xylene isomers (Herman et al., 1991). A benzene concentration of 73,600 ktg/L interferes with reproduction in the macroalga Champia parvula (Thursby and Steele, 1986). Some species or life stages of marine animals are much more sensitive than others. For example, bay shrimp Cragofranciscorum and juvenile striped bass Morone saxatilis are quite sensitive to BTEX (Benville and Kom, 1977), whereas others, such mosquitofish Gambusia affinis are extremely tolerant (Wallen et al., 1957). Rotifers Brachionus calcyciflorus and B plicatilis are extremely tolerant (Ferrando and Andreu-Moliner, 1992). 24-hr LCs0s range from 113,300 to 552,600 ktg/L for toluene and xylene, and B. plicatilis is more tolerant than B. cacyciflorus. Benzene at concentrations as high as 1,000,000/~g/L is without effects on the rotifers.

Table 87. Geometric mean LCs0s (48-hour exposure or greater) for several monocyclic aromatic hydrocarbons based on available data from the AQUIRE database (EPA, 1997). Concentrations are/Jg/L.

Chemical Benzene Toluene Ethylbenzene o-Xylene m-Xylene p-Xylene Propylbenzene 1,2,4-Trimethylbenzene 1,3,5-Trimethylbenzene 1,3-Diethylbenzene 1,2,4,5-Tetramethylbenzene

Log Kow 2.13 2.65 3.13 3.18 3.20 3.13 3.69 3.60 3.58 4.10 4.10

Geometric Mean LCs0 35,420

27,320 19,020 10,950 8,570 2,900 1,500 5,280 4,150 4,150 470

238 Bioaccumulation in Marine Organisms Much of the apparent differences in sensitivity of freshwater and marine organisms to BTEX may be caused by differences in toxicity test methods. BTEX are extremely difficult to maintain at constant concentrations in exposure media. If exposure concentrations are not measured regularly, it is not possible to estimate actual exposure concentrations or dose (exposure concentration x duration of exposure). In addition, the dose/response curve for BTEX is extremely steep, meaning that small differences in actual exposure concentration or duration have a marked effect of response. For example, the 96-hr LC50 for benzene in juvenile striped bass is 10,900 ktg/L (Meyerhoff, 1975). However, an exposure concentration of 10,000 ~tg/L is without acute effects and a concentration of 20,000 ktg/L causes 50 percent mortality in about two hours. The steep dose/response curve is caused by the very rapid rates of uptake and release of BTEX by freshwater and marine organisms. The mechanisms of acute BTEX toxicity to marine organisms are thought to include nonspecific narcosis and alterations of permeability of cell membranes, particularly in the gills (Meyerhoff, 1975; Morrow et al., 1975); both responses can be attributed to absorption of BTEX into lipid-rich cell membranes, causing membrane swelling and eventually disruption (Abernethy et al., 1986, 1988). BTEX may also cause developmental defects. Sea urchin Paracentrotus lividus embryos experience an increased incidence of developmental defects and metaphase/anaphase abnormalities when exposed to 78 ~tg/L benzene (Pagano et al., 1988). Exposure to different xylene isomers at concentrations of 2,000 to 7,000/zg/L causes abnormal early cell division in fertilized eggs of cod Gadus morhua (Kjorsvik et al., 1982). o-Xylene appears to be less toxic than m- and p-xylenes. Monocyclic aromatic hydrocarbons also inhibit metamorphosis to the polyp stage of free-swimming larvae of the marine hydroid Hydractinia echinata; there is an inverse relationship between aromatic hydrocarbon molecular weight and toxicity to the hydroids (Chicu and Barking, 1997). The marine acute water quality criteria for benzene, toluene, and ethylbenzene are 5,100, 6,300, and 430 ktg/L, respectively (Table 30). The chronic criteria for benzene and toluene are 700 and 5,000/zg/L, respectively. These values actually are no observed effects concentrations; there are insufficient data to develop criteria. There are no freshwater or marine water quality criteria for xylenes; the drinking water criterion is 10,000/zg/L. There also is no chronic value for ethylbenzene. Benzene is a known human carcinogen, based on several studies of an increased incidence of nonlymphocytic leukemia from occupational exposure, and increased incidence of neoplasia in rodents following inhalation and oral exposure (Snyder et al., 1981; Rinsky et al., 1987). The cancers attributed to benzene inhalation by humans include myelogenous leukemia, chronic lymphatic leukemia, and lymphatic and hematopoietic cancers (Hughes et al., 1994; Legator, 1997; NCEA-W, 1998). Benzene also is a skin irritant, causing dermatitis following long-term exposure (Clayton and Clayton, 1982). Inhalation of benzene produces adverse effects in the central nervous system and gastrointestinal tract (Gilman et al., 1985). Chronic exposure may lead to aplastic anemia and a tendency to hemorrhage, eventually leading to an onset of leukemia (Grant, 1986). The toxicity of benzene to mammals is attributed to hydroquinone and ring-breakage metabolites produced in the liver and other organs (Henderson, 1996). The inhalation risk-based concentration (RBC) is 0.22 ~tg/m3 (EPA, 2000). There is no evidence that any other monocyclic aromatic hydrocarbons are carcinogenic in animals and humans (IARC, 1989). Toluene has a moderate systemic toxicity to

Chapter 14 - Monocyclic Aromatic Hydrocarbons in the Ocean 239

humans. Inhalation of large doses of toluene, as in glue sniffing, may cause metabolic acidosis, electrolyte abnormalities, muscle weakness, and cardiac arrhythmias (Hamilton and Hardy, 1974). It has an inhalation RBC of 420/tg/m 3 (EPA, 2000). Ethylbenzene and xylenes have a low systemic toxicity. They have inhalation RBCs of 1,100/zg/m 3 and 7,300/tg/m 3, respectively (EPA, 2000). The human health criteria (fish consumption) for benzene, toluene, and ethylbenzene are 40, 424,000, and 3,280 pg/L, respectively. The low human health criterion for benzene is due to the fact that it is a known mammalian carcinogen (Fishbein, 1984; Medinsky et al., 1994). The RBC for benzene in food is 1.14 pg/g wet wt (5.7/tg/g dry wt) (Table 30). However, food is not a quantitatively important pathway for human or other mammalian bioaccumulation of benzene (Wallace, 1996). Most bioaccumulation in humans is from inhalation of cigarette smoke and automobile exhaust. RBCs are much higher for toluene, ethylbenzene and xylenes, ranging from 1,350 /zg/g dry wt for ethylbenzene to 27,035/tg/g for xylenes. These concentrations in tissues of marine animals are unlikely because of the low persistence of BTEX in seawater, and the rapid elimination of any accumulated BTEX from tissues of marine animals. 14.7 ENVIRONMENTAL EFFECTS O F M O N O C Y C L I C AROMATIC H Y D R O C A R B O N S IN P R O D U C E D WATER Although concentrations of total benzene, toluene, ethylbenzene, and xylenes (BTEX) often are greater than 10,000 pg/L in treated produced water, these compounds dilute very rapidly in the receiving water environment following discharge of produced water to the ocean. The water quality criteria for individual monocyr162 aromatic hydrocarbons, intended to protect marine organisms and their consumers, including man, are virtually never exceeded in marine waters near produced water discharges. It may be possible to attain a concentration of 40/zg/L benzene in solution under a slick of crude or refined petroleum for a short period of time (hours) after an oil spill. Elevated concentrations of BTEX have been reported in shallow, poorly-mixed estuarine and fresh waters receiving large-volume produced water discharges. However, high concentrations are not likely to persist long enough to contaminate fishery products to a level possibly harmful to human consumers. The main route of uptake of benzene and other BTEX by humans is via inhalation, particularly by smoking cigarettes (Fishbein, 1984, 1985a,b,c; Hallenbeck and Flowers, 1992; Hughes et al., 1994; Meek and Chan, 1994b,r Food and drinking water represent only a very minor source to man of these highly volatile chemicals. There are no reports in the scientific literature of BTEX concentrations in edible tissues of marine animals that are higher than the RBC. Whipple (1979) did report concentrations of total BTEX up to nearly 29/zg/g dry wt in liver of striped bass from San Francisco Bay. This is the highest concentration ever reported and may be anomalous. Based on published data for other marine animals, it is highly likely that all or nearly all the BTEX in the bass livers was toluene, ethylbenzene, and xylenes, which have much higher risk based concentrations and screening values. Most of the fish, crabs, and bivalve mollusks collected near offshore produced waterdischarging and non-discharging platforms in the Gulf of Mexico did not contain detectable concentrations of benzene, toluene, or ethylbenzene (Offshore Operators Committee, 1997a,b). More than 95 percent of the marine animals sampled contained

240 Bioaccumulation in Marine Organisms less than 0.003/tg/g dry wt benzene, toluene, and ethylbenzene. The highest concentrations of benzene, toluene, and ethylbenzene detected in fish muscle tissue were 0.023 /tg/g, 0.046/tg/g, and 0.030/tg/g, respectively. Bivalves contained up to 0.015/tg/g benzene, 0.068/tg/g toluene, and 0.011/tg/g ethylbenzene. Blue crabs Callinectes sapidus contained up to 0.014/tg/g benzene and 0.019/tg/g toluene. Therefore, BTEX in produced water and seawater pose a minimal risk to marine animals themselves or their consumers, including man.