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Photo-oxidation and Photo-toxicity of Crude and Refined Oils
Spill Science & Technology Bulletin, Vol. 8, No. 2, pp. 157–162, 2003 Ó 2003 Elsevier Science Ltd. All rights reserved Printed in Great Britain 1353-2561/03 $ - see front matter
doi:10.1016/S1353-2561(03)00015-X
Photo-oxidation and Photo-toxicity of Crude and Refined Oils RICHARD F. LEE* Skidaway Institute of Oceanography, 10 Ocean Science Circle, University System of Georgia, Savannah, GA 31411, USA
The fate and effects of an oil spill are effected by solar radiation through the action of photo-oxidation and photo-toxicity. Photo-oxidation, an important process in the weathering of oil, produces a variety of oxidized compounds, including aliphatic and aromatic ketones, aldehydes, carboxylic acids, fatty acids, esters, epoxides, sulfoxides, sulfones, phenols, anhydrides, quinones and aliphatic and aromatic alcohols. Some of these compounds contribute to the marine biota toxicity observed after an oil spill. Photo-toxicity occurs when uptake of certain petroleum compounds, e.g. certain polycyclic aromatic hydrocarbons and benzothiophenes, is followed by solar exposure which results in much greater toxicity than after dark uptake. The mechanism of PAH photo-toxicity includes absorbance of solar radiation by the PAH which produces a free radical and this free radical in turn reacts with oxygen to produce reactive oxygen species that can damage DNA and other cellular macromolecules. While most studies on photo-toxicity have been carried out in the laboratory, there are studies showing that water from an oil spill is photo-toxic to bivalve embryos for at least a few days after the spill. Other studies have found that oil contaminated sediments are photo-toxic to several marine invertebrates. More studies are required to determine if marine fauna at an oil spill site are effected by the action of photo-toxicity and photo-oxidation. Ó 2003 Elsevier Science Ltd. All rights reserved. Keywords: Ultraviolet, toxicity, oil, hydrocarbons, photolysis, photo-oxidation
Introduction This review discusses how the weathering and toxicity of an oil spill is affected by solar radiation through photo-oxidation and photo-toxicity. Photooxidation, one of the processes important in the weathering of oil, produces a variety of oxidized compounds. These compounds, because of their high polarity and water solubility contribute to the disappearance of an oil slick. Photo-oxidation products also contribute to the toxicity of some weathered oils. Photo-toxicity is where solar exposure after uptake by marine organisms of certain petroleum compounds, e.g. PAHs, benzothiophenes, results in much greater toxicity than when there is dark uptake. The portion
*Tel.: +1-912-598-2494; fax: +1-912-598-2310. E-mail address: [email protected] (R.F. Lee).
of the solar spectrum responsible for both photooxidation and photo-toxicity is primarily the ultraviolet regions which for the earthÕs surface is composed of 5% UV-B (280–315 nm) and 95% UV-A (315–400 nm).
Photo-oxidation of an Oil Spill Conditions around oil slicks in coastal waters includes highly oxygenated water and intense solar radiation at the slickÕs surface. These conditions lead to photo-oxidation of the slick, which results in the production of a variety of oxygenated hydrocarbons and sulfur compounds, including aliphatic and aromatic ketones, aldehydes, carboxylic acids, fatty acids, esters, epoxides, sulfoxides, sulfones, phenols, anhydrides, quinones and aliphatic and aromatic alcohols (Burwood & Speers, 1974; Hansen, 1975; Larson et al., 157
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(300 and 500 nm) found in solar radiation. There is photo-oxidation of PAHs in the water or adsorbed to suspended particulates. The rate of direct photolysis of PAHs can be described by the equation developed by Zepp and Cline (1977) dPAHd =dt ¼ /ka ½PAHd where / ¼ a molar yield coefficient, ka ¼ the sum of the kak values for all wavelengths (k) of sunlight absorbed by the PAH, PAHd ¼ concentration of dissolved PAH (lmoles/l). Reported yield coefficients ranged between 0.001 and 0.01 for polycyclic aromatic hydrocarbons (Zepp & Schlotzheuer, 1979). A linear regression based on data in Zepp and Schlotzheuer (1979) related molecular weight to molar yield coefficient. / ¼ 0:0235–8:38 105 molecular weight
Fig. 1 Examples of photo-oxidized compounds produced by the action of solar radiation on an oil slick.
1977, 1979; Overton et al., 1980; Patel et al., 1979; Payne & Phillips, 1985) (Fig. 1). Many of these photooxidized compounds are much more rapidly degraded by resident microbes in the water than the parent compounds (Lee, 1980; Lee et al., 1982; Rontani et al., 1987; National Academy of Sciences, 1985). Freegarde et al. (1971) determined that solar radiation destroyed a Kuwait oil slick (2.5 lm layer) in 100 h. Presumably this destruction was due to a combination of microbial degradation and photo-oxidation. Besides the effects on surface slicks, photo-oxidation can also act on petroleum components in the water, including dissolved hydrocarbons, dispersed oil droplets and water-in-oil emulsions. Two studies which identified photo-oxidation products in the water after an oil spill were the following: (1) benzothiophene sulfoxides were identified in the water after solar radiation had acted on the Amoco Cadiz spill (Calder et al., 1978; Patel et al., 1979) (2) anthraquinone found in the water after oil spills from the 1991 Gulf War was assumed to be produced by photo-oxidation of anthracene in the oil slicks (Ehrhardt & Burns, 1993). The mechanism of photo-oxidation of petroleum hydrocarbon includes both direct photolysis and also the reaction of reactive oxygen species produced by solar radiation acting on a variety of photo-sensitizers in natural waters (Mill et al., 1980; Zepp & Baughman, 1978). Direct photolysis is largely responsible for degradation of higher weight PAHs, since many of them absorb light in ultraviolet or visible wavelengths 158
Using information on the attenuation of solar radiation in natural waters, a depth-specific rate of photolysis of PAHs can be calculated (Bartell et al., 1981). In addition to water soluble photo-oxidation products, there can also be large insoluble polymers produced by photo-initiated free radical reactions acting on an oil slick (Thominette & Verdu, 1984). Photo-oxidation products with amphipathic properties and photo-produced polymers contribute to the formation and stability of water-in-oil emulsions (Cormack, 1999). Stable and persistent emulsions with their increased density and viscosity can make for difficult cleanup operations.
Toxicity of Photo-oxidation Products When sunlight acts on petroleum the toxicity to marine life can be increased. The various hydroperoxides, phenols, carboxylic acids and ketones, which are produced as a result of solar radiation on oil slicks, are thought to be the cause of the observed toxicity of photo-oxidized oil (Hansen, 1975; Herbes & Whitley, 1983; Larson et al., 1976, 1977, 1979; National Academy of Sciences, 1985; Winters et al., 1977) (Fig. 1). Phenalen-1-one and 9-fluorenone, found in the water around oil slicks exposed to solar radiation, was toxic to various microalgae species (Winters et al., 1977) while the photo-oxidation products, benz(a) anthraquinone and benzanthrone, were toxic to aquatic animals (Fernandez & LÕHaridon, 1992; Oris & Giesy, 1987). Phenanthrenequinone, a photo-oxidation product of phenanthrene, was significantly more toxic than phenanthrene to the marine bacteria, Photo-bacterium phosphoreum (McConkey et al., 1997). Photo-oxidized anthracene, benzo(a)pyrene, fluoranthene, phenanthSpill Science & Technology Bulletin 8(2)
PHOTO-OXIDATION AND PHOTO-TOXICITY OF CRUDE AND REFINED OILS
rene and pyrene were more toxic to the duckweed, Lemna gibba, than the parent compounds (Huang et al., 1995). In addition to toxicity studies with pure compounds, there have also been several studies testing the toxicity of photo-oxidized oils. Exposure of various estuarine fish and invertebrate species to both solar radiation and a water soluble fraction of a fuel oil (#2) increased the toxicity compared with dark exposure to this fuel oil (Scheier & Gominger, 1976). The water soluble fraction from Kuwait crude oil exposed to solar radiation was found to be three times more toxic to the microalgae, Phaeooactylum tricornutum, compared with dark exposure (Lacaze & Villedon de Naide, 1976). The photo-products produced after exposure of Ekofisk and Statfjord crude oil to sunlight were found to affect microbial activity indicators (incorporation of C14-labeled amino acids, glucose and thymidine) of natural assemblages of marine bacteria (Pengerud et al., 1984). However not all studies have found toxicity after oils are exposed to solar radiation. Van der Linden (1978) tested the water soluble photo-oxidation products of a crude oil exposed to solar radiation and did find not any evidence of toxic effects of these products on bacterial cultures. Some possible explanations for the lack to toxicity observed in this latter study may be due to microbial degradation of photo-oxidation products, insufficient time of radiation exposure to produce toxic photo-products, or resistance of these bacterial cultures to the photo-products. It should be noted that many photo-oxidation products are unstable and others are quickly degraded by resident microbes. Due to rapid degradation, it seems likely that photo-oxidation products would contribute to the toxicity of an oil spill for only 1 or 2 days.
Photo-toxicity There is a large body of literature showing that the toxicity of certain PAHs is greatly enhanced when there is exposure to both PAHs and sunlight. In addition to mortality, there are also studies showing that exposure to sunlight and PAHs caused a variety of sub-lethal effects in marine animals (Boese et al., 1998, 2000; Duesterloh et al., in press). The mechanism of PAH photo-toxicity includes absorbance of solar radiation by the PAH which produces a free radical and this free radical in turn reacts with oxygen to produce reactive oxygen species, e.g. superoxide radical anion, that can damage DNA and other cellular macromolecules. If photo-ionization occurs after PAHs or their derivatives bind to DNA then the free radicals produced can react with adjacent nucleotide bases (Blackburn & Taussig, 1975; Gasper & Schuster, 1997; Osborne & Crosby, 1987; Strniste et al., 1980). A Spill Science & Technology Bulletin 8(2)
quantitative structure-activity relationship model has been developed to predict which compounds, e.g. PAHs, alkylated PAHs, benzothiophenes, will show photo-toxicity (Mekenyan et al., 1994; Swartz et al., 1997; Veith et al., 1995). This model correlates phototoxicity with the HOMO-LUMO gap which is the energy difference between the highest occupied molecular orbital and the lowest unoccupied molecular orbital. The compounds with the most photo-toxic potential have HOMO-LUMO gaps in the range of 6.5–8.0 eV with a maximum effect near 7.1 eV. Table 1 shows the HOMO-LUMO gaps for some compounds commonly found in petroleum. Anthracene, fluoranthene, pyrene and dibenzothiophene in both sediment and water have been shown to be photo-toxic to a variety of vertebrate and invertebrate aquatic life (Ankley et al., 1995; Boese et al., 1997, 1998; Holst & Giesy, 1989; Kagan et al., 1985; Kosian et al., 1998; Landrum et al., 1984; Mekenyan et al., 1994; Oris & Giesy, 1985; Pelletier et al., 1997; Stevens et al., 1999; Swartz et al., 1997; Weinstein & Oris, 1999). In addition to work with specific compounds there have also been laboratory studies on the phototoxicity of water accommodated oils or with sediments containing oil (Table 2). Fish (tidewater silverside, Menidia beryllina) exposed for 48 h in the dark to a water accommodated fraction (WAF) of weathered middle distillate oil (1.5 mg/l of total petroleum hydrocarbons) showed no toxicity, however exposure to the WAF and solar radiation (48 h) resulted in 30% toxicity (Little et al., 2000). Kosian et al. (1998) tested various fractions of sediment pore water contaminated with oil refinery discharge for photo-toxicity to the freshwater oligochaete, Lumbriculus variegatus. Benzothiophenes, benzacridines, quinolines, benzanthracenes, benzopyrenes and aminopyrenes were some of the photo-toxic compounds found in photo-toxic fractions. A recent study found increased mortality and impairment of swimming ability by the calanoid
Table 1 HOMO-LUMO gap energies for compounds found in petroleuma Compound Anthracene Benzo(a)pyrene Fluoranthene Pyrene Benz(a)anthracene Naphthalene Chrysene Fluorene Phenanthrene Dibenzothiophene
HOMO-LUMO Photo-toxic (Yes or No) gap energies (eV) 7.3 6.8 7.7 7.2 7.4 10.1 7.7 8.5 8.2 7.9
Yes Yes Yes Yes Yes No No No No Yes
a Compounds with the most photo-toxic potential have HOMOLUMO gaps in the range of 6.5–8.0 eV.
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Table 2 Photo-toxicity of water accomodated fraction (WAF) of oils to marine organisms solar lamps (S) or fluorescent lamp (F) or darkness (D) were used to test the photo-toxicity of the WAF from the different oils Oil (WAF)
Species tested
S/F/D
Exposure time (days)
Sub-lethal test (lg/l)
EC50 (lg/l)
Weathered oil Weathered oil Weathered oil Weathered oil Weathered oil Arabian crude Arabian crude Prudhoe crude Prudhoe crude Fuel oil #6 Fuel oil #6 Arabian crude
M. beryllina M. beryllina M. beryllina M. bahia M. bahia M. bahia M. bahia M. bahia M. bahia M. bahia M. bahia M. lateralis
S S F S F S F S F S F S
4 7 7 7 7 2 2 2 2 2 2 3
– – – – – – – – – – – 8
Arabian crude
M. lateralis
F
3
Prudhoe crude
M. lateralis
S
3
Prudhoe crude
M. lateralis
F
3
Fuel oil #6
M. lateralis
S
3
Fuel oil #6
M. lateralis
F
3
– – – – – – – – – – – Growth and development Growth and development Growth and development Growth and development Growth and development Growth and development
LC50 (mg/l or lg/l)
Reference
1.1 (TPHs) Little et al. (2000) 0.5 (TPHs) Little et al. (2000) 2.8 (TPHs) Little et al. (2000) 0.4 (TPHs) Cleveland et al. (2000) 0.9 (TPHs) Cleveland et al. (2000) 28 (PAHs) Pelletier et al. (1997) 140 (PAHs) Pelletier et al. (1997) 87 (PAHs) Pelletier et al. (1997) 160 (PAHs) Pelletier et al. (1997) 20 (PAHs) Pelletier et al. (1997) 1500 (PAHs) Pelletier et al. (1997) – Pelletier et al. (1997)
120
–
Pelletier et al. (1997)
87
–
Pelletier et al. (1997)
>2500
–
Pelletier et al. (1997)
20
–
Pelletier et al. (1997)
1500
–
Pelletier et al. (1997)
LC50s were either based on total petroleum hydrocarbons (TPHs) concentrations in mg/l or total polycyclic aromatic hydrocarbons (PAHs) concentrations in lg/l. EC50s were based on PAH concentrations in lg/l. Species tested included a fish (silverside, Menidia beryllina), a mysid shrimp (Mysidopsis bahia) and bivalve embryos (Mulinia lateralis). References for the studies were Little et al. (2000); Cleveland et al. (2000); Pelletier et al. (1997).
copepods, Calanus marshallae and Metridia okhotensis, exposed to solar ultraviolet and water-soluble fractions of weathered Alaska North Slope crude oil compared to animals exposed to oil in the dark (Duesterloh et al., in press). Photo-toxicity studies with water accommodated fraction of oil in the laboratory does not replicate many of the conditions found at an oil spill, including differences in dilution and mixing energy. There are a few studies suggesting that photo-toxicity does occur in the field. Ho et al. (1999) determined that water collected after a fuel oil spill off Rhode Island was photo-toxic in the laboratory to bivalve embryos. Embryos were all killed after exposure to water from the spill area spill for 48 h, including 16 h exposure in a solar simulator (UVA––300 lW/cm2 ; UVB––110 lW/cm2 ). Thirteen days after the spill the water from the area was no longer photo-toxic. Thus this work shows that the water from a spill area, at least for a few days after the spill, has potential photo-toxicity. Other studies found both mortality and sub-lethal effects in oligochaetes (Lumbriculus variegatus) and amphipods (Rhepoxynius abronius, Leptocheirus plumulosus) exposed to petroleum-contaminated sediments along with solar radiation (Boese et al., 2000; Monson et al., 1995). To assess the importance of photo-toxicity after an actual oil spill, I suggest some additional studies: (1) 160
collection of animals from an oil spill site followed by exposure to solar radiation and assessment of subsequent toxicity or sub-lethal effects compared with controls; (2) determine the photo-toxicity with petroleum containing water or sediments to animals at different water depths, since ultraviolet radiation is rapidly attenuated in most natural waters (Barron et al., 2000; Barron & KaÕaihue, 2001; Landrum et al., 1984).
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Spill Science & Technology Bulletin 8(2)
doi:10.1016/S1353-2561(03)00015-X
Photo-oxidation and Photo-toxicity of Crude and Refined Oils RICHARD F. LEE* Skidaway Institute of Oceanography, 10 Ocean Science Circle, University System of Georgia, Savannah, GA 31411, USA
The fate and effects of an oil spill are effected by solar radiation through the action of photo-oxidation and photo-toxicity. Photo-oxidation, an important process in the weathering of oil, produces a variety of oxidized compounds, including aliphatic and aromatic ketones, aldehydes, carboxylic acids, fatty acids, esters, epoxides, sulfoxides, sulfones, phenols, anhydrides, quinones and aliphatic and aromatic alcohols. Some of these compounds contribute to the marine biota toxicity observed after an oil spill. Photo-toxicity occurs when uptake of certain petroleum compounds, e.g. certain polycyclic aromatic hydrocarbons and benzothiophenes, is followed by solar exposure which results in much greater toxicity than after dark uptake. The mechanism of PAH photo-toxicity includes absorbance of solar radiation by the PAH which produces a free radical and this free radical in turn reacts with oxygen to produce reactive oxygen species that can damage DNA and other cellular macromolecules. While most studies on photo-toxicity have been carried out in the laboratory, there are studies showing that water from an oil spill is photo-toxic to bivalve embryos for at least a few days after the spill. Other studies have found that oil contaminated sediments are photo-toxic to several marine invertebrates. More studies are required to determine if marine fauna at an oil spill site are effected by the action of photo-toxicity and photo-oxidation. Ó 2003 Elsevier Science Ltd. All rights reserved. Keywords: Ultraviolet, toxicity, oil, hydrocarbons, photolysis, photo-oxidation
Introduction This review discusses how the weathering and toxicity of an oil spill is affected by solar radiation through photo-oxidation and photo-toxicity. Photooxidation, one of the processes important in the weathering of oil, produces a variety of oxidized compounds. These compounds, because of their high polarity and water solubility contribute to the disappearance of an oil slick. Photo-oxidation products also contribute to the toxicity of some weathered oils. Photo-toxicity is where solar exposure after uptake by marine organisms of certain petroleum compounds, e.g. PAHs, benzothiophenes, results in much greater toxicity than when there is dark uptake. The portion
*Tel.: +1-912-598-2494; fax: +1-912-598-2310. E-mail address: [email protected] (R.F. Lee).
of the solar spectrum responsible for both photooxidation and photo-toxicity is primarily the ultraviolet regions which for the earthÕs surface is composed of 5% UV-B (280–315 nm) and 95% UV-A (315–400 nm).
Photo-oxidation of an Oil Spill Conditions around oil slicks in coastal waters includes highly oxygenated water and intense solar radiation at the slickÕs surface. These conditions lead to photo-oxidation of the slick, which results in the production of a variety of oxygenated hydrocarbons and sulfur compounds, including aliphatic and aromatic ketones, aldehydes, carboxylic acids, fatty acids, esters, epoxides, sulfoxides, sulfones, phenols, anhydrides, quinones and aliphatic and aromatic alcohols (Burwood & Speers, 1974; Hansen, 1975; Larson et al., 157
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(300 and 500 nm) found in solar radiation. There is photo-oxidation of PAHs in the water or adsorbed to suspended particulates. The rate of direct photolysis of PAHs can be described by the equation developed by Zepp and Cline (1977) dPAHd =dt ¼ /ka ½PAHd where / ¼ a molar yield coefficient, ka ¼ the sum of the kak values for all wavelengths (k) of sunlight absorbed by the PAH, PAHd ¼ concentration of dissolved PAH (lmoles/l). Reported yield coefficients ranged between 0.001 and 0.01 for polycyclic aromatic hydrocarbons (Zepp & Schlotzheuer, 1979). A linear regression based on data in Zepp and Schlotzheuer (1979) related molecular weight to molar yield coefficient. / ¼ 0:0235–8:38 105 molecular weight
Fig. 1 Examples of photo-oxidized compounds produced by the action of solar radiation on an oil slick.
1977, 1979; Overton et al., 1980; Patel et al., 1979; Payne & Phillips, 1985) (Fig. 1). Many of these photooxidized compounds are much more rapidly degraded by resident microbes in the water than the parent compounds (Lee, 1980; Lee et al., 1982; Rontani et al., 1987; National Academy of Sciences, 1985). Freegarde et al. (1971) determined that solar radiation destroyed a Kuwait oil slick (2.5 lm layer) in 100 h. Presumably this destruction was due to a combination of microbial degradation and photo-oxidation. Besides the effects on surface slicks, photo-oxidation can also act on petroleum components in the water, including dissolved hydrocarbons, dispersed oil droplets and water-in-oil emulsions. Two studies which identified photo-oxidation products in the water after an oil spill were the following: (1) benzothiophene sulfoxides were identified in the water after solar radiation had acted on the Amoco Cadiz spill (Calder et al., 1978; Patel et al., 1979) (2) anthraquinone found in the water after oil spills from the 1991 Gulf War was assumed to be produced by photo-oxidation of anthracene in the oil slicks (Ehrhardt & Burns, 1993). The mechanism of photo-oxidation of petroleum hydrocarbon includes both direct photolysis and also the reaction of reactive oxygen species produced by solar radiation acting on a variety of photo-sensitizers in natural waters (Mill et al., 1980; Zepp & Baughman, 1978). Direct photolysis is largely responsible for degradation of higher weight PAHs, since many of them absorb light in ultraviolet or visible wavelengths 158
Using information on the attenuation of solar radiation in natural waters, a depth-specific rate of photolysis of PAHs can be calculated (Bartell et al., 1981). In addition to water soluble photo-oxidation products, there can also be large insoluble polymers produced by photo-initiated free radical reactions acting on an oil slick (Thominette & Verdu, 1984). Photo-oxidation products with amphipathic properties and photo-produced polymers contribute to the formation and stability of water-in-oil emulsions (Cormack, 1999). Stable and persistent emulsions with their increased density and viscosity can make for difficult cleanup operations.
Toxicity of Photo-oxidation Products When sunlight acts on petroleum the toxicity to marine life can be increased. The various hydroperoxides, phenols, carboxylic acids and ketones, which are produced as a result of solar radiation on oil slicks, are thought to be the cause of the observed toxicity of photo-oxidized oil (Hansen, 1975; Herbes & Whitley, 1983; Larson et al., 1976, 1977, 1979; National Academy of Sciences, 1985; Winters et al., 1977) (Fig. 1). Phenalen-1-one and 9-fluorenone, found in the water around oil slicks exposed to solar radiation, was toxic to various microalgae species (Winters et al., 1977) while the photo-oxidation products, benz(a) anthraquinone and benzanthrone, were toxic to aquatic animals (Fernandez & LÕHaridon, 1992; Oris & Giesy, 1987). Phenanthrenequinone, a photo-oxidation product of phenanthrene, was significantly more toxic than phenanthrene to the marine bacteria, Photo-bacterium phosphoreum (McConkey et al., 1997). Photo-oxidized anthracene, benzo(a)pyrene, fluoranthene, phenanthSpill Science & Technology Bulletin 8(2)
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rene and pyrene were more toxic to the duckweed, Lemna gibba, than the parent compounds (Huang et al., 1995). In addition to toxicity studies with pure compounds, there have also been several studies testing the toxicity of photo-oxidized oils. Exposure of various estuarine fish and invertebrate species to both solar radiation and a water soluble fraction of a fuel oil (#2) increased the toxicity compared with dark exposure to this fuel oil (Scheier & Gominger, 1976). The water soluble fraction from Kuwait crude oil exposed to solar radiation was found to be three times more toxic to the microalgae, Phaeooactylum tricornutum, compared with dark exposure (Lacaze & Villedon de Naide, 1976). The photo-products produced after exposure of Ekofisk and Statfjord crude oil to sunlight were found to affect microbial activity indicators (incorporation of C14-labeled amino acids, glucose and thymidine) of natural assemblages of marine bacteria (Pengerud et al., 1984). However not all studies have found toxicity after oils are exposed to solar radiation. Van der Linden (1978) tested the water soluble photo-oxidation products of a crude oil exposed to solar radiation and did find not any evidence of toxic effects of these products on bacterial cultures. Some possible explanations for the lack to toxicity observed in this latter study may be due to microbial degradation of photo-oxidation products, insufficient time of radiation exposure to produce toxic photo-products, or resistance of these bacterial cultures to the photo-products. It should be noted that many photo-oxidation products are unstable and others are quickly degraded by resident microbes. Due to rapid degradation, it seems likely that photo-oxidation products would contribute to the toxicity of an oil spill for only 1 or 2 days.
Photo-toxicity There is a large body of literature showing that the toxicity of certain PAHs is greatly enhanced when there is exposure to both PAHs and sunlight. In addition to mortality, there are also studies showing that exposure to sunlight and PAHs caused a variety of sub-lethal effects in marine animals (Boese et al., 1998, 2000; Duesterloh et al., in press). The mechanism of PAH photo-toxicity includes absorbance of solar radiation by the PAH which produces a free radical and this free radical in turn reacts with oxygen to produce reactive oxygen species, e.g. superoxide radical anion, that can damage DNA and other cellular macromolecules. If photo-ionization occurs after PAHs or their derivatives bind to DNA then the free radicals produced can react with adjacent nucleotide bases (Blackburn & Taussig, 1975; Gasper & Schuster, 1997; Osborne & Crosby, 1987; Strniste et al., 1980). A Spill Science & Technology Bulletin 8(2)
quantitative structure-activity relationship model has been developed to predict which compounds, e.g. PAHs, alkylated PAHs, benzothiophenes, will show photo-toxicity (Mekenyan et al., 1994; Swartz et al., 1997; Veith et al., 1995). This model correlates phototoxicity with the HOMO-LUMO gap which is the energy difference between the highest occupied molecular orbital and the lowest unoccupied molecular orbital. The compounds with the most photo-toxic potential have HOMO-LUMO gaps in the range of 6.5–8.0 eV with a maximum effect near 7.1 eV. Table 1 shows the HOMO-LUMO gaps for some compounds commonly found in petroleum. Anthracene, fluoranthene, pyrene and dibenzothiophene in both sediment and water have been shown to be photo-toxic to a variety of vertebrate and invertebrate aquatic life (Ankley et al., 1995; Boese et al., 1997, 1998; Holst & Giesy, 1989; Kagan et al., 1985; Kosian et al., 1998; Landrum et al., 1984; Mekenyan et al., 1994; Oris & Giesy, 1985; Pelletier et al., 1997; Stevens et al., 1999; Swartz et al., 1997; Weinstein & Oris, 1999). In addition to work with specific compounds there have also been laboratory studies on the phototoxicity of water accommodated oils or with sediments containing oil (Table 2). Fish (tidewater silverside, Menidia beryllina) exposed for 48 h in the dark to a water accommodated fraction (WAF) of weathered middle distillate oil (1.5 mg/l of total petroleum hydrocarbons) showed no toxicity, however exposure to the WAF and solar radiation (48 h) resulted in 30% toxicity (Little et al., 2000). Kosian et al. (1998) tested various fractions of sediment pore water contaminated with oil refinery discharge for photo-toxicity to the freshwater oligochaete, Lumbriculus variegatus. Benzothiophenes, benzacridines, quinolines, benzanthracenes, benzopyrenes and aminopyrenes were some of the photo-toxic compounds found in photo-toxic fractions. A recent study found increased mortality and impairment of swimming ability by the calanoid
Table 1 HOMO-LUMO gap energies for compounds found in petroleuma Compound Anthracene Benzo(a)pyrene Fluoranthene Pyrene Benz(a)anthracene Naphthalene Chrysene Fluorene Phenanthrene Dibenzothiophene
HOMO-LUMO Photo-toxic (Yes or No) gap energies (eV) 7.3 6.8 7.7 7.2 7.4 10.1 7.7 8.5 8.2 7.9
Yes Yes Yes Yes Yes No No No No Yes
a Compounds with the most photo-toxic potential have HOMOLUMO gaps in the range of 6.5–8.0 eV.
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Table 2 Photo-toxicity of water accomodated fraction (WAF) of oils to marine organisms solar lamps (S) or fluorescent lamp (F) or darkness (D) were used to test the photo-toxicity of the WAF from the different oils Oil (WAF)
Species tested
S/F/D
Exposure time (days)
Sub-lethal test (lg/l)
EC50 (lg/l)
Weathered oil Weathered oil Weathered oil Weathered oil Weathered oil Arabian crude Arabian crude Prudhoe crude Prudhoe crude Fuel oil #6 Fuel oil #6 Arabian crude
M. beryllina M. beryllina M. beryllina M. bahia M. bahia M. bahia M. bahia M. bahia M. bahia M. bahia M. bahia M. lateralis
S S F S F S F S F S F S
4 7 7 7 7 2 2 2 2 2 2 3
– – – – – – – – – – – 8
Arabian crude
M. lateralis
F
3
Prudhoe crude
M. lateralis
S
3
Prudhoe crude
M. lateralis
F
3
Fuel oil #6
M. lateralis
S
3
Fuel oil #6
M. lateralis
F
3
– – – – – – – – – – – Growth and development Growth and development Growth and development Growth and development Growth and development Growth and development
LC50 (mg/l or lg/l)
Reference
1.1 (TPHs) Little et al. (2000) 0.5 (TPHs) Little et al. (2000) 2.8 (TPHs) Little et al. (2000) 0.4 (TPHs) Cleveland et al. (2000) 0.9 (TPHs) Cleveland et al. (2000) 28 (PAHs) Pelletier et al. (1997) 140 (PAHs) Pelletier et al. (1997) 87 (PAHs) Pelletier et al. (1997) 160 (PAHs) Pelletier et al. (1997) 20 (PAHs) Pelletier et al. (1997) 1500 (PAHs) Pelletier et al. (1997) – Pelletier et al. (1997)
120
–
Pelletier et al. (1997)
87
–
Pelletier et al. (1997)
>2500
–
Pelletier et al. (1997)
20
–
Pelletier et al. (1997)
1500
–
Pelletier et al. (1997)
LC50s were either based on total petroleum hydrocarbons (TPHs) concentrations in mg/l or total polycyclic aromatic hydrocarbons (PAHs) concentrations in lg/l. EC50s were based on PAH concentrations in lg/l. Species tested included a fish (silverside, Menidia beryllina), a mysid shrimp (Mysidopsis bahia) and bivalve embryos (Mulinia lateralis). References for the studies were Little et al. (2000); Cleveland et al. (2000); Pelletier et al. (1997).
copepods, Calanus marshallae and Metridia okhotensis, exposed to solar ultraviolet and water-soluble fractions of weathered Alaska North Slope crude oil compared to animals exposed to oil in the dark (Duesterloh et al., in press). Photo-toxicity studies with water accommodated fraction of oil in the laboratory does not replicate many of the conditions found at an oil spill, including differences in dilution and mixing energy. There are a few studies suggesting that photo-toxicity does occur in the field. Ho et al. (1999) determined that water collected after a fuel oil spill off Rhode Island was photo-toxic in the laboratory to bivalve embryos. Embryos were all killed after exposure to water from the spill area spill for 48 h, including 16 h exposure in a solar simulator (UVA––300 lW/cm2 ; UVB––110 lW/cm2 ). Thirteen days after the spill the water from the area was no longer photo-toxic. Thus this work shows that the water from a spill area, at least for a few days after the spill, has potential photo-toxicity. Other studies found both mortality and sub-lethal effects in oligochaetes (Lumbriculus variegatus) and amphipods (Rhepoxynius abronius, Leptocheirus plumulosus) exposed to petroleum-contaminated sediments along with solar radiation (Boese et al., 2000; Monson et al., 1995). To assess the importance of photo-toxicity after an actual oil spill, I suggest some additional studies: (1) 160
collection of animals from an oil spill site followed by exposure to solar radiation and assessment of subsequent toxicity or sub-lethal effects compared with controls; (2) determine the photo-toxicity with petroleum containing water or sediments to animals at different water depths, since ultraviolet radiation is rapidly attenuated in most natural waters (Barron et al., 2000; Barron & KaÕaihue, 2001; Landrum et al., 1984).
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