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Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay
Marine Pollution Bulletin xxx (2014) xxx–xxx
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay Jiro Koyama a,⇑, Chie Imakado a, Seiichi Uno a, Takako Kuroda b, Shouichi Hara b, Takahiro Majima b, Hideyuki Shirota b, Nathaniel C. Añasco c a b c
Faculty of Fisheries, Kagoshima University, 4-50-20 Shimoarata, Kagoshima, Japan National Maritime Research Institute, 6-38-1, Shinkawa, Mitaka, Tokyo, Japan Institute of Marine Fisheries and Oceanology, College of Fisheries and Ocean Sciences, University of the Philippines Visayas, Miagao, Iloilo 5023, Philippines
a r t i c l e
i n f o
Keywords: Simulation Dispersed oil Ecotoxicity-based Marine organisms
a b s t r a c t To assess risks of chemically-dispersed oil to marine organisms, oil concentrations in the water were simulated using a hypothetical spill accident in Tokyo Bay. Simulated oil concentrations were then compared with the short-term no-observed effect concentration (NOEC), 0.01 mg/L, obtained through toxicity tests using marine diatoms, amphipod and fish. Area of oil concentrations higher than the NOEC were compared with respect to use and non-use of dispersant. Results of the simulation show relatively faster dispersion near the mouth of the bay compared to its inner sections which is basically related to its stronger water currents. Interestingly, in the inner bay, a large area of chemically-dispersed oil has concentrations higher than the NOEC. It seems emulsifying oil by dispersant increases oil concentrations, which could lead to higher toxicity to aquatic organisms. When stronger winds occur, however, the difference in toxic areas between use and non-use of dispersant is quite small. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Large oil spill accidents around the world such as the 2002 Prestige in the Coast of Galicia (Europe) and the 2010 Deepwater Horizon in the Gulf of Mexico (North America) are feared to happen again in the future (Jernelöv, 2010). Spilled oil at sea most often hit coastal areas and, consequently, adversely affects aquatic organisms as reported in Exxon Valdez oil spill accident (Brown et al., 1996; Hose et al., 1996). Hence, dispersants have been applied frequently to disperse spilled oil quickly (Charles and Schmidt, 2010; Lessard and Demarco, 2000). First generation dispersants, nevertheless, were mixtures of kerosene and other chemicals that are toxic to human and aquatic organisms (Charles and Schmidt, 2010; Lessard and Demarco, 2000). In the case of Torrey Canyon, for instance, application of dispersants even led to subsequent widespread damage (Lessard and Demarco, 2000). Fortunately, modern dispersants are already mixtures of less toxic solvents and surfactants. However, application of dispersant to spilled oil as an effective counter-measure in the environment still needs to be clarified. Several researches have pointed out some adverse effects of the mixture of spilled oil and dispersant to aquatic organisms based on laboratory experiments ⇑ Corresponding author. Tel.: +81 99 286 4743; fax: +81 99 286 4296. E-mail address: koyama@fish.kagoshima-u.ac.jp (J. Koyama).
(Koyama and Kakuno, 2004; Fisher and Foss, 1993; Middaugh and Whiting, 1995; Singer et al., 1998; Adams et al., 1999). Hence, the NOAA/API guidelines generally recommend applying dispersants only in open waters and large rivers with sufficient depth and volume for dilution (SL Ross Environmental Research, 2010). Other than direct contact to oil, dissolved oil also has adverse and acute effects on aquatic organisms particularly pelagic fishes and invertebrates (French-McCay, 2004). Yet in most simulation studies, models have predicted only distribution of oil slick or dispersed oil (Guo and Wang, 2009; Zhang et al., 1997; Sugioka et al., 1999). So there is a need for a study that will show all at the same time simulation of distribution of dissolved oil concentrations in the water, determination of the no-observed effect concentration with and without application of dispersant and assessment of risks posed by chemically-dispersed oil to marine organisms. This study, therefore, aimed to address this gap by examining the differences of toxic areas (oil concentrations higher than the NOEC) between simulated oil distributions in spills with and without application of dispersants. 2. Materials and methods 2.1. Simulation of spilled oil distribution in Tokyo Bay The distribution of dissolved oil concentrations in the water of 0.25 km2 at depths of 0–1 m after a hypothetical oil spill accident
http://dx.doi.org/10.1016/j.marpolbul.2014.04.001 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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involving 2000 tons of heavy oil in Tokyo Bay was simulated by a model using a decision-making process tool for oil pollution on GIS (DOG, Shirota et al., 2009) shown in Fig. 1. Moreover, dispersion process of the spilled oil is represented by a number of particles (Shen et al., 1986). The particles are scattered by sea surface currents and dispersed by eddy diffusivity. The spreading model presented by Fay (1969) was used for each particle to compute its surface area. Fig. 2 shows schematic drawing of the oil dissolution process. In the model used for this study, the dissolution process is separated into two elements, i.e. dissolution for the oil on the sea surface and dissolution for the oil droplet in the water column (Shirota et al., 2009). In addition, efficiency of emulsification of the dispersant was assumed to be 40% as per information from the manufacturer. To determine variations in the distribution of oil concentrations as influenced by unique characteristics of potential sites of actual spill, hypothetical oil spills were simulated in four stations around Tokyo Bay as shown in Fig. 3. 2.2. Test organisms Acute toxicities of heavy fuel oil WAF and DWAF were examined using four kinds of marine organisms that are found in coastal waters of Japan. Test organisms were: two species of diatoms (Chaetoceros gracilis and Skeletonema costatum), juveniles of an amphipod (Hyale barbicornis), and embryo of red sea bream (Pagrus major). C. gracilis, S. costatum and H. barbicornis are currently being reared in our laboratory for use in toxicity testing. Newly-spawned embryo of P. major were purchased from a public hatchery in Kagoshima, Japan. These test organisms have been used for some ecotoxicity tests in Japan (Koyama and Kakuno, 2004; Añasco et al., 2008). 2.3. Exposure to WAF and DWAF Water-accommodated fraction of oil was prepared following the protocols of Singer et al. (2000). Briefly, 100 mL of heavy C oil was mixed at 200 rpm with 0.9 L of seawater for 23 h and settled for 1 h. After separating from oil, water was collected by glass siphon. The collected water was used as WAF. On the other hand, 100 mL of heavy C oil, 0.9 L of seawater and 2.64 g of dispersant (D1128, Taiho Kogyo; 3% of oil weight as recommended by the manufacturer) were mixed for 18 h in 1 L glass beaker at 360 rpm and settled for 6 h. After separating, water was collected by glass siphon and was used as chemically-dispersed accommodated fraction (DWAF). For exposure experiments involving diatoms, ESP medium was added to the seawater (Provasoli, 1968). Diatoms were exposed to several concentrations of WAF and DWAF for 72 h with population growths monitored using the in vivo fluorescence intensity (EX: 437 nm, EM: 676 nm) to
Fig. 2. Schematic drawing of the dissolution process of spilled oil.
determine inhibition of growth rates following Van der Heever and Grobbelaar (1998). Two-week old amphipod juveniles were exposed to several concentrations of WAF and DWAF for 96 h. Test waters (WAF and DWAF) were replaced with newly prepared ones after 48 h. Changes in swimming behavior were monitored every day. Fish embryos were exposed to several concentrations of WAF and DWAF until hatched. Since it took only 2 d for fish embryos to hatch, test waters were not replaced. Immediately after hatching, fish larva was examined for any malformation. Using inhibition of growth rates in diatoms, immobility in amphipods and malformation in fish larvae, the median effective concentration (EC50) and no-observed effect concentration (EC10) were estimated. These values were calculated by probit method.
2.4. Determination of oil concentrations Since majority of oil toxicity has been reported to be caused by polyaromatic hydrocarbons (PAHs) and monoaromatics (FrenchMcCay, 2004), total oil concentration, which is primarily a reflection of the complex mixture of compounds containing 2 or more aromatic rings (Koyama and Kakuno, 2004), was measured by fluorescence as recommended by the Intergovernmental Oceanographic Commission (IOC, 1984). Briefly, oil concentration of test water was analyzed by fluorescence spectrophotometer (EX: 310 nm, EM: 360 nm) after extraction by n-hexane using chrysene as a standard. In addition, concentrations of specific PAHs were determined following Uno et al. (2010). Briefly, test waters were extracted twice by hexane and dichloromethane (1:1, v/v). After dehydration using anhydrous sodium hydrate and concentration under nitrogen (N2) gas, extracts were loaded onto a silica-gel column (moisture 3%) for clean up then PAHs were eluted by hexane and 1% acetone–hexane. After concentration under N2 gas, PAHs in the extracts were analyzed by GC/MS (Agilent 6890 GC equipped with Agilent 5973 MSD). All oil and PAH concentrations were geometric mean of measured concentrations.
(8) Oil Dispersant Application (Mass of Toxic Ingredient in Oil on Sea Surface x Efficiency)
Oil on Sea Surface Surface Area
(5 )
Dissolution Amount of Toxic Ingredient from Oil on Sea Surface
Wind Velocity Mixing Depth
(6 )
Total Dissolution Amount of Toxic Ingredient
(1), (2), (3) (7) Amount of Oil Droplet in Water Column
(4 )
Dissolution Amount of Toxic Ingredient from Oil Dro plet in Water Column
Concentration of Toxic Ingredient (Amount of Toxic Ingredient/ Cell Volume )
Fig. 1. Flow chart for calculating the concentration of toxic component of spilled oil.
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
J. Koyama et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
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St.1 St.2 St.3
St.4
Fig. 3. Map of the study area (Tokyo Bay, Japan).
Explanation and discussion were done based on oil concentrations by fluorescence, except for Table 1 where PAH concentrations were shown.
3. Results and discussion
2.5. Risk assessment
The oil concentrations of water column from 0 to 1 m depth were simulated after a hypothetical spill of 2000 tons of heavy oil at Stations 1, 2, 3 and 4 in Tokyo Bay. It was observed that oil concentrations were generally higher in the inner portions of the bay and when dispersants are not applied to the spilled oil. For instance, Fig. 4 shows a comparison of the simulated distribution of oil concentrations at Station 1 where higher concentrations are
Toxic areas, defined as areas with oil concentration higher than the estimated NOEC, between simulations with and without application of dispersants were compared by Student’s t-test at the significant level of p < 0.05 to assess risks posed by chemically-dispersed oil to marine organisms.
3.1. Prediction of dissolved oil concentrations
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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Table 1 Measured PAHs and alkPAHs concentrations at 40% WAF for red sea bream toxicity experiment. PAHs
Mean concentrations (|lg/L)
Naphthalene Acenaphthylene Acenaphthene Fluorene Dibenzothiophene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[a] anthracene Chrysene Benzo[b] fluoranthene Benzo[k] fluoranthene Benzo[a] pyrene Perylene Benzo[g.h.i]perylene Dibenzo[a.h] anthracene Indeno[1.2.3-c.d] pyrene
35.6 0.01 0.10 0.25 0.23 0.16 0.04 ND (<0.01) ND ND ND ND ND ND ND ND ND ND
alkPAHs
Mean concentrations (|lg/L)
1-Methyl naphthalene 2-Methyl naphthalene 1.2-Dimethyl naphthalene 2.3.5-Trimethyl naphtharene 1-Methyl fluorene 4-Methyl dibenzothiophene 4.6-Dimethyl dibenzothiophene 2-Methyl phenanthrene 1-Methyl phenanthrene 1-Methyl anthracene 2.3-Dimethyl anthracene 2-Methyl fluoranthene 1-Methyl pyrene 1-Methyl benzo[a] anthracene 7.12-Dimethyl benzo[a] anthracene 4-Methyl chrysene 7-Methyl benzo[a]pyrene
9.24 25.3 0.31 0.07 0.06 0.04 ND (<0.01) 0.15 ND 0.02 ND ND ND ND ND ND ND
observed in an oil spill treated with a dispersant (A) than when a dispersant was not applied (B). However, whether these concentrations are toxic or not is unknown unless an ecotoxicity-based assessment is conducted. As guide in determination of potential sources of oil toxicity, the mean PAHs and alkyl PAH concentrations of 40% WAF for red sea bream toxicity test are shown in Table 1.
3.2. Toxicities of WAF and DWAF on marine organisms At first the toxicity of the dispersant used was assessed to justify its application in the simulated oil spill. Results show that the median lethal concentration (LC50) of the dispersant (D1128) used in this study was higher than 1000 mg/L for red sea bream embryo. However, according to Koyama and Kakuno (2004), LC50s of many dispersants for marine fish are lower than 1000 mg (lL)/L. This suggests, therefore, that D1128 has low toxicity to marine organisms. Since the National Research Council (2003) pointed out that soluble oil components contribute to acute toxicity, this study focused on the acute toxicity to aquatic organisms after oil spill. Based on the results of growth inhibition of diatoms, immobilization of juvenile amphipods, and higher occurrence of abnormality in fish larvae, EC50 and EC10 of WAF and DWAF of heavy oil were estimated as shown in Table 2. Estimated EC50 values in this study are similar to previous studies using heavy or weathered oil such as the reported LC50 of total petroleum hydrocarbons (TPH) in WAF of fuel oil and Bunker C oil were 0.9–4.9 mg/L for some
Fig. 4. Predicted distribution of dissolved oil concentration without dispersant (A) and with dispersant (B) 24 h after heavy oil spill (2000 ton) at St.1 (d). Wind direction: North, wind speed: 2.5 m/s. The area of each grid is 0.25 km2.
Table 2 EC50 and EC10 of oil for marine organisms (mg/L). Test organisms
WAF
DWAF
EC50
EC10
EC50
EC10
Chaetoceros gracilis Skeletonema costatum
0.39 0.1
0.1 0.03
0.35 0.34
0.03 0.17
Amphipod Hyale barbicornis
0.09
0.05
0.06
0.04
Fish Pagrus major
0.11
0.08
0.018
0.004
Phytoplankton
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cumulative proportion (%)
Fig. 5. Newly-hatched fish larvae (A): control and (B): fish larvae exposed to WAF.
100 90 80 70 60 50 40 30 20 10 0 0.001
0.01
0.1
1
EC10, EC50 (mg/L) Fig. 6. Percentage of abnormality in fish larvae exposed to WAF.
Fig. 7. Cumulative proportion of EC10 and EC50 of oil for marine organisms exposed to WAF and DWAF. Closed and open marks showed EC10 and EC50, respectively.
Fig. 8. Comparison of areas showing oil concentration higher than 0.01 mg/L 24 h after oil spill without and with dispersant at North wind of 1 m/s. : Significantly different (p < 0.05).
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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et al., 1999) reported spinal malformation in herring larvae exposed to weathered crude oil with EC50 higher than 3.6 lg/L. Exposure to oil induces malformations in fish larvae such as spinal malformation even at lower concentrations. Therefore, red sea bream also induced spinal malformation at similar lower oil concentrations (EC50 and EC10 ranged from 0.004 to 0.11 mg/L). Except for EC10 of DWAF for red sea bream, all EC50s and EC10s were higher than 0.018 mg/L. In some studies, EC10s were recommended to use in order to assess the risks of chemicals (Warne and van Dam, 2008; Landis and Chapman, 2011). Accordingly, as shown in the cumulative proportion of these EC50s and EC10s (Fig. 7), the short-term no-observed effect concentration is approximated at 0.01 mg/L.
3.3. Risks on marine organisms
Fig. 9. Speed of water current at North wind of 1 m/s.
shrimps (Anderson et al., 1974) and EC50 TPH of weathered crude oil for larval herring malformation was 3.6 lg/L (Carls et al., 1999). In the fish experiment, all embryos hatched but some exposed to WAF or DWAF exhibited deformities as shown in Figs. 5 and 6. All deformed fish showed curvature of vertebrae and did not survive after a few days from hatching. This observation is consistent with reports showing malformation in fish larvae that were exposed to oil such as cod larvae to TPH 0.245 mg/L of crude oil (Tilseth et al., 1984) and crimson-spotted rainbow fish to > TPH 0.5 mg/ L of crude oil (Pollino and Holdway, 2002). Another study (Carls
The total toxic area which showed oil concentration higher than the short-term no-observed effect oil concentration were estimated in both simulated spill scenarios involving use and nonuse of dispersant. As shown in Fig. 8, predicted toxic areas showing oil concentrations higher than 0.01 mg/L were larger in the inner parts of the bay (Stations 1 and 2) than the mouth of the bay (Stations 3 and 4) after application of dispersant at wind speed of 1 m/ s. This is in agreement with the findings of Broch et al. (2013) that oil concentrations were higher in areas with weaker water currents and within the expected pattern of water movement inside Tokyo Bay (shown in Fig. 9) at wind speed of 1 m/s. In the mouth of the bay, no significant differences were observed between application and no application of dispersant. Sometimes lower oil concentrations were even observed after application of dispersant. As reported by Koyama and Kakuno (2004) and Middaugh and Whiting (1995), the application of dispersant to spilled oil leads to temporary increase in oil concentration because of emulsification. Consequently, this results in increased adverse effects to aquatic organisms. Moreover, simulations suggest that the application of dispersant causes an increase in the toxic areas brought by less exchange of seawater and as a consequence higher risks of spilled oil in the inner parts of the bay. However, toxic areas were
Fig. 10. Comparison of areas showing oil higher than 0.01 mg/L 24 h after oil spill without and with dispersant at North wind of 7.5 m/s. : Significantly different (p < 0.05).
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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relatively smaller in the mouth of the bay due to faster dispersion of emulsified oil. To determine influence of water currents on oil concentrations and its toxicity to marine organisms, wind speed was increased to 7.5 m/s (shown in Fig. 10). Results show that the predicted toxic areas were larger in the inner parts of the bay (Stations 1 and 2) compared to the mouth of the bay (Stations 3 and 4) regardless of application or non-application of dispersant. Although significantly larger toxic areas were predicted after application of dispersant in Station 4 than non-application, toxic areas were generally smaller compared to the other stations. Moreover, in Station 3 smaller toxic areas were predicted after application of dispersant. While strong wind seems to enhance dispersion of oil in inner sections of the bay that lead to no difference in distribution of oil concentrations between application and non-application of dispersants, the same strong winds seem to facilitate faster natural spreading of chemically-dispersed oil that led to smaller toxic areas after dispersant application. 4. Conclusions Based on the ecotoxicity experiments using diatoms, juveniles of an amphipod and fish embryo of red sea bream, the short-term no-observed effect concentration of oil (EC10 of each experiment) was estimated at 0.01 mg/L. While application of dispersant does not contribute to any toxicity, emulsifying oil by dispersants will increase dissolved oil concentration that can automatically increase the toxic areas around the spilled oil. Moreover, the risk of emulsified and dispersed oil is expected to increase in areas with weaker water current such as in the inner parts of Tokyo Bay. Meanwhile, the risk is expected to decrease in areas with stronger water current such as near the mouth of the bay. Thus, it can be concluded that the level of risk posed by chemically-dispersed oil to marine organisms is similar to non-application of dispersants with regards to the toxic area except when winds are too weak to enhance natural dispersal of spilled oil. References Adams, G.G., Klerks, P.L., Belanger, S.E., Dantin, D., 1999. The effects of the oil dispersant omni-clean on the toxicity of fuel oil No. 2 in two bioassays with the sheepshead minnow Cyprinodon variegates. Chemosphere 39, 2141–2157. Añasco, N.C., Koyama, J., Imai, S., Nakamura, K., 2008. Toxicity of residual chlorines from hypochlorite-treated seawater to marine amphipod Hyale barbicornis and estuarine fish Oryzias javanicus. Water Air Soil Pollut. 195, 129–136. Anderson, J.W., Neff, J.M., Cox, B.A., Tatem, H.E., Hightower, G.M., 1974. Characteristics of dispersants and water–soluble extractions of crude and refined oils and their toxicity to estuarine crustaceans and fish. Mar. Biol. 27, 75–88. Broch, O.J., Slagstad, D., Smit, M., 2013. Modelling produced water dispersion and its direct toxic effects on the production and biomass of the marine copepod Calanus finmarchicus. Mar. Environ. Res. 84, 84–95. Brown, E.D., Norcross, B.L., Short, J.W., 1996. An introduction to studies on the effects of the Exxon Valdez oil spill on early life history stages of Pacific herring, Clupea pallasi, in Prince William sound. Alaska Can. J. Fish. Aquat. Sci. 53, 2337– 2342. Carls, M.G., Rice, S.D., Hose, J.E., 1999. Sensitivity of fish embryos to weathered crude oil: part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval pacifi herring (Clupea pallasi). Environ. Toxicol. Chem. 18, 481–493. Charles, W., Schmidt, M.S., 2010. Between the devil and the deep blue sea: dispersants in the gulf of mexico. Environ. Health Persp. 228 (8), A338–A344.
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay Jiro Koyama a,⇑, Chie Imakado a, Seiichi Uno a, Takako Kuroda b, Shouichi Hara b, Takahiro Majima b, Hideyuki Shirota b, Nathaniel C. Añasco c a b c
Faculty of Fisheries, Kagoshima University, 4-50-20 Shimoarata, Kagoshima, Japan National Maritime Research Institute, 6-38-1, Shinkawa, Mitaka, Tokyo, Japan Institute of Marine Fisheries and Oceanology, College of Fisheries and Ocean Sciences, University of the Philippines Visayas, Miagao, Iloilo 5023, Philippines
a r t i c l e
i n f o
Keywords: Simulation Dispersed oil Ecotoxicity-based Marine organisms
a b s t r a c t To assess risks of chemically-dispersed oil to marine organisms, oil concentrations in the water were simulated using a hypothetical spill accident in Tokyo Bay. Simulated oil concentrations were then compared with the short-term no-observed effect concentration (NOEC), 0.01 mg/L, obtained through toxicity tests using marine diatoms, amphipod and fish. Area of oil concentrations higher than the NOEC were compared with respect to use and non-use of dispersant. Results of the simulation show relatively faster dispersion near the mouth of the bay compared to its inner sections which is basically related to its stronger water currents. Interestingly, in the inner bay, a large area of chemically-dispersed oil has concentrations higher than the NOEC. It seems emulsifying oil by dispersant increases oil concentrations, which could lead to higher toxicity to aquatic organisms. When stronger winds occur, however, the difference in toxic areas between use and non-use of dispersant is quite small. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Large oil spill accidents around the world such as the 2002 Prestige in the Coast of Galicia (Europe) and the 2010 Deepwater Horizon in the Gulf of Mexico (North America) are feared to happen again in the future (Jernelöv, 2010). Spilled oil at sea most often hit coastal areas and, consequently, adversely affects aquatic organisms as reported in Exxon Valdez oil spill accident (Brown et al., 1996; Hose et al., 1996). Hence, dispersants have been applied frequently to disperse spilled oil quickly (Charles and Schmidt, 2010; Lessard and Demarco, 2000). First generation dispersants, nevertheless, were mixtures of kerosene and other chemicals that are toxic to human and aquatic organisms (Charles and Schmidt, 2010; Lessard and Demarco, 2000). In the case of Torrey Canyon, for instance, application of dispersants even led to subsequent widespread damage (Lessard and Demarco, 2000). Fortunately, modern dispersants are already mixtures of less toxic solvents and surfactants. However, application of dispersant to spilled oil as an effective counter-measure in the environment still needs to be clarified. Several researches have pointed out some adverse effects of the mixture of spilled oil and dispersant to aquatic organisms based on laboratory experiments ⇑ Corresponding author. Tel.: +81 99 286 4743; fax: +81 99 286 4296. E-mail address: koyama@fish.kagoshima-u.ac.jp (J. Koyama).
(Koyama and Kakuno, 2004; Fisher and Foss, 1993; Middaugh and Whiting, 1995; Singer et al., 1998; Adams et al., 1999). Hence, the NOAA/API guidelines generally recommend applying dispersants only in open waters and large rivers with sufficient depth and volume for dilution (SL Ross Environmental Research, 2010). Other than direct contact to oil, dissolved oil also has adverse and acute effects on aquatic organisms particularly pelagic fishes and invertebrates (French-McCay, 2004). Yet in most simulation studies, models have predicted only distribution of oil slick or dispersed oil (Guo and Wang, 2009; Zhang et al., 1997; Sugioka et al., 1999). So there is a need for a study that will show all at the same time simulation of distribution of dissolved oil concentrations in the water, determination of the no-observed effect concentration with and without application of dispersant and assessment of risks posed by chemically-dispersed oil to marine organisms. This study, therefore, aimed to address this gap by examining the differences of toxic areas (oil concentrations higher than the NOEC) between simulated oil distributions in spills with and without application of dispersants. 2. Materials and methods 2.1. Simulation of spilled oil distribution in Tokyo Bay The distribution of dissolved oil concentrations in the water of 0.25 km2 at depths of 0–1 m after a hypothetical oil spill accident
http://dx.doi.org/10.1016/j.marpolbul.2014.04.001 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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involving 2000 tons of heavy oil in Tokyo Bay was simulated by a model using a decision-making process tool for oil pollution on GIS (DOG, Shirota et al., 2009) shown in Fig. 1. Moreover, dispersion process of the spilled oil is represented by a number of particles (Shen et al., 1986). The particles are scattered by sea surface currents and dispersed by eddy diffusivity. The spreading model presented by Fay (1969) was used for each particle to compute its surface area. Fig. 2 shows schematic drawing of the oil dissolution process. In the model used for this study, the dissolution process is separated into two elements, i.e. dissolution for the oil on the sea surface and dissolution for the oil droplet in the water column (Shirota et al., 2009). In addition, efficiency of emulsification of the dispersant was assumed to be 40% as per information from the manufacturer. To determine variations in the distribution of oil concentrations as influenced by unique characteristics of potential sites of actual spill, hypothetical oil spills were simulated in four stations around Tokyo Bay as shown in Fig. 3. 2.2. Test organisms Acute toxicities of heavy fuel oil WAF and DWAF were examined using four kinds of marine organisms that are found in coastal waters of Japan. Test organisms were: two species of diatoms (Chaetoceros gracilis and Skeletonema costatum), juveniles of an amphipod (Hyale barbicornis), and embryo of red sea bream (Pagrus major). C. gracilis, S. costatum and H. barbicornis are currently being reared in our laboratory for use in toxicity testing. Newly-spawned embryo of P. major were purchased from a public hatchery in Kagoshima, Japan. These test organisms have been used for some ecotoxicity tests in Japan (Koyama and Kakuno, 2004; Añasco et al., 2008). 2.3. Exposure to WAF and DWAF Water-accommodated fraction of oil was prepared following the protocols of Singer et al. (2000). Briefly, 100 mL of heavy C oil was mixed at 200 rpm with 0.9 L of seawater for 23 h and settled for 1 h. After separating from oil, water was collected by glass siphon. The collected water was used as WAF. On the other hand, 100 mL of heavy C oil, 0.9 L of seawater and 2.64 g of dispersant (D1128, Taiho Kogyo; 3% of oil weight as recommended by the manufacturer) were mixed for 18 h in 1 L glass beaker at 360 rpm and settled for 6 h. After separating, water was collected by glass siphon and was used as chemically-dispersed accommodated fraction (DWAF). For exposure experiments involving diatoms, ESP medium was added to the seawater (Provasoli, 1968). Diatoms were exposed to several concentrations of WAF and DWAF for 72 h with population growths monitored using the in vivo fluorescence intensity (EX: 437 nm, EM: 676 nm) to
Fig. 2. Schematic drawing of the dissolution process of spilled oil.
determine inhibition of growth rates following Van der Heever and Grobbelaar (1998). Two-week old amphipod juveniles were exposed to several concentrations of WAF and DWAF for 96 h. Test waters (WAF and DWAF) were replaced with newly prepared ones after 48 h. Changes in swimming behavior were monitored every day. Fish embryos were exposed to several concentrations of WAF and DWAF until hatched. Since it took only 2 d for fish embryos to hatch, test waters were not replaced. Immediately after hatching, fish larva was examined for any malformation. Using inhibition of growth rates in diatoms, immobility in amphipods and malformation in fish larvae, the median effective concentration (EC50) and no-observed effect concentration (EC10) were estimated. These values were calculated by probit method.
2.4. Determination of oil concentrations Since majority of oil toxicity has been reported to be caused by polyaromatic hydrocarbons (PAHs) and monoaromatics (FrenchMcCay, 2004), total oil concentration, which is primarily a reflection of the complex mixture of compounds containing 2 or more aromatic rings (Koyama and Kakuno, 2004), was measured by fluorescence as recommended by the Intergovernmental Oceanographic Commission (IOC, 1984). Briefly, oil concentration of test water was analyzed by fluorescence spectrophotometer (EX: 310 nm, EM: 360 nm) after extraction by n-hexane using chrysene as a standard. In addition, concentrations of specific PAHs were determined following Uno et al. (2010). Briefly, test waters were extracted twice by hexane and dichloromethane (1:1, v/v). After dehydration using anhydrous sodium hydrate and concentration under nitrogen (N2) gas, extracts were loaded onto a silica-gel column (moisture 3%) for clean up then PAHs were eluted by hexane and 1% acetone–hexane. After concentration under N2 gas, PAHs in the extracts were analyzed by GC/MS (Agilent 6890 GC equipped with Agilent 5973 MSD). All oil and PAH concentrations were geometric mean of measured concentrations.
(8) Oil Dispersant Application (Mass of Toxic Ingredient in Oil on Sea Surface x Efficiency)
Oil on Sea Surface Surface Area
(5 )
Dissolution Amount of Toxic Ingredient from Oil on Sea Surface
Wind Velocity Mixing Depth
(6 )
Total Dissolution Amount of Toxic Ingredient
(1), (2), (3) (7) Amount of Oil Droplet in Water Column
(4 )
Dissolution Amount of Toxic Ingredient from Oil Dro plet in Water Column
Concentration of Toxic Ingredient (Amount of Toxic Ingredient/ Cell Volume )
Fig. 1. Flow chart for calculating the concentration of toxic component of spilled oil.
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St.1 St.2 St.3
St.4
Fig. 3. Map of the study area (Tokyo Bay, Japan).
Explanation and discussion were done based on oil concentrations by fluorescence, except for Table 1 where PAH concentrations were shown.
3. Results and discussion
2.5. Risk assessment
The oil concentrations of water column from 0 to 1 m depth were simulated after a hypothetical spill of 2000 tons of heavy oil at Stations 1, 2, 3 and 4 in Tokyo Bay. It was observed that oil concentrations were generally higher in the inner portions of the bay and when dispersants are not applied to the spilled oil. For instance, Fig. 4 shows a comparison of the simulated distribution of oil concentrations at Station 1 where higher concentrations are
Toxic areas, defined as areas with oil concentration higher than the estimated NOEC, between simulations with and without application of dispersants were compared by Student’s t-test at the significant level of p < 0.05 to assess risks posed by chemically-dispersed oil to marine organisms.
3.1. Prediction of dissolved oil concentrations
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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Table 1 Measured PAHs and alkPAHs concentrations at 40% WAF for red sea bream toxicity experiment. PAHs
Mean concentrations (|lg/L)
Naphthalene Acenaphthylene Acenaphthene Fluorene Dibenzothiophene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[a] anthracene Chrysene Benzo[b] fluoranthene Benzo[k] fluoranthene Benzo[a] pyrene Perylene Benzo[g.h.i]perylene Dibenzo[a.h] anthracene Indeno[1.2.3-c.d] pyrene
35.6 0.01 0.10 0.25 0.23 0.16 0.04 ND (<0.01) ND ND ND ND ND ND ND ND ND ND
alkPAHs
Mean concentrations (|lg/L)
1-Methyl naphthalene 2-Methyl naphthalene 1.2-Dimethyl naphthalene 2.3.5-Trimethyl naphtharene 1-Methyl fluorene 4-Methyl dibenzothiophene 4.6-Dimethyl dibenzothiophene 2-Methyl phenanthrene 1-Methyl phenanthrene 1-Methyl anthracene 2.3-Dimethyl anthracene 2-Methyl fluoranthene 1-Methyl pyrene 1-Methyl benzo[a] anthracene 7.12-Dimethyl benzo[a] anthracene 4-Methyl chrysene 7-Methyl benzo[a]pyrene
9.24 25.3 0.31 0.07 0.06 0.04 ND (<0.01) 0.15 ND 0.02 ND ND ND ND ND ND ND
observed in an oil spill treated with a dispersant (A) than when a dispersant was not applied (B). However, whether these concentrations are toxic or not is unknown unless an ecotoxicity-based assessment is conducted. As guide in determination of potential sources of oil toxicity, the mean PAHs and alkyl PAH concentrations of 40% WAF for red sea bream toxicity test are shown in Table 1.
3.2. Toxicities of WAF and DWAF on marine organisms At first the toxicity of the dispersant used was assessed to justify its application in the simulated oil spill. Results show that the median lethal concentration (LC50) of the dispersant (D1128) used in this study was higher than 1000 mg/L for red sea bream embryo. However, according to Koyama and Kakuno (2004), LC50s of many dispersants for marine fish are lower than 1000 mg (lL)/L. This suggests, therefore, that D1128 has low toxicity to marine organisms. Since the National Research Council (2003) pointed out that soluble oil components contribute to acute toxicity, this study focused on the acute toxicity to aquatic organisms after oil spill. Based on the results of growth inhibition of diatoms, immobilization of juvenile amphipods, and higher occurrence of abnormality in fish larvae, EC50 and EC10 of WAF and DWAF of heavy oil were estimated as shown in Table 2. Estimated EC50 values in this study are similar to previous studies using heavy or weathered oil such as the reported LC50 of total petroleum hydrocarbons (TPH) in WAF of fuel oil and Bunker C oil were 0.9–4.9 mg/L for some
Fig. 4. Predicted distribution of dissolved oil concentration without dispersant (A) and with dispersant (B) 24 h after heavy oil spill (2000 ton) at St.1 (d). Wind direction: North, wind speed: 2.5 m/s. The area of each grid is 0.25 km2.
Table 2 EC50 and EC10 of oil for marine organisms (mg/L). Test organisms
WAF
DWAF
EC50
EC10
EC50
EC10
Chaetoceros gracilis Skeletonema costatum
0.39 0.1
0.1 0.03
0.35 0.34
0.03 0.17
Amphipod Hyale barbicornis
0.09
0.05
0.06
0.04
Fish Pagrus major
0.11
0.08
0.018
0.004
Phytoplankton
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cumulative proportion (%)
Fig. 5. Newly-hatched fish larvae (A): control and (B): fish larvae exposed to WAF.
100 90 80 70 60 50 40 30 20 10 0 0.001
0.01
0.1
1
EC10, EC50 (mg/L) Fig. 6. Percentage of abnormality in fish larvae exposed to WAF.
Fig. 7. Cumulative proportion of EC10 and EC50 of oil for marine organisms exposed to WAF and DWAF. Closed and open marks showed EC10 and EC50, respectively.
Fig. 8. Comparison of areas showing oil concentration higher than 0.01 mg/L 24 h after oil spill without and with dispersant at North wind of 1 m/s. : Significantly different (p < 0.05).
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et al., 1999) reported spinal malformation in herring larvae exposed to weathered crude oil with EC50 higher than 3.6 lg/L. Exposure to oil induces malformations in fish larvae such as spinal malformation even at lower concentrations. Therefore, red sea bream also induced spinal malformation at similar lower oil concentrations (EC50 and EC10 ranged from 0.004 to 0.11 mg/L). Except for EC10 of DWAF for red sea bream, all EC50s and EC10s were higher than 0.018 mg/L. In some studies, EC10s were recommended to use in order to assess the risks of chemicals (Warne and van Dam, 2008; Landis and Chapman, 2011). Accordingly, as shown in the cumulative proportion of these EC50s and EC10s (Fig. 7), the short-term no-observed effect concentration is approximated at 0.01 mg/L.
3.3. Risks on marine organisms
Fig. 9. Speed of water current at North wind of 1 m/s.
shrimps (Anderson et al., 1974) and EC50 TPH of weathered crude oil for larval herring malformation was 3.6 lg/L (Carls et al., 1999). In the fish experiment, all embryos hatched but some exposed to WAF or DWAF exhibited deformities as shown in Figs. 5 and 6. All deformed fish showed curvature of vertebrae and did not survive after a few days from hatching. This observation is consistent with reports showing malformation in fish larvae that were exposed to oil such as cod larvae to TPH 0.245 mg/L of crude oil (Tilseth et al., 1984) and crimson-spotted rainbow fish to > TPH 0.5 mg/ L of crude oil (Pollino and Holdway, 2002). Another study (Carls
The total toxic area which showed oil concentration higher than the short-term no-observed effect oil concentration were estimated in both simulated spill scenarios involving use and nonuse of dispersant. As shown in Fig. 8, predicted toxic areas showing oil concentrations higher than 0.01 mg/L were larger in the inner parts of the bay (Stations 1 and 2) than the mouth of the bay (Stations 3 and 4) after application of dispersant at wind speed of 1 m/ s. This is in agreement with the findings of Broch et al. (2013) that oil concentrations were higher in areas with weaker water currents and within the expected pattern of water movement inside Tokyo Bay (shown in Fig. 9) at wind speed of 1 m/s. In the mouth of the bay, no significant differences were observed between application and no application of dispersant. Sometimes lower oil concentrations were even observed after application of dispersant. As reported by Koyama and Kakuno (2004) and Middaugh and Whiting (1995), the application of dispersant to spilled oil leads to temporary increase in oil concentration because of emulsification. Consequently, this results in increased adverse effects to aquatic organisms. Moreover, simulations suggest that the application of dispersant causes an increase in the toxic areas brought by less exchange of seawater and as a consequence higher risks of spilled oil in the inner parts of the bay. However, toxic areas were
Fig. 10. Comparison of areas showing oil higher than 0.01 mg/L 24 h after oil spill without and with dispersant at North wind of 7.5 m/s. : Significantly different (p < 0.05).
Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001
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relatively smaller in the mouth of the bay due to faster dispersion of emulsified oil. To determine influence of water currents on oil concentrations and its toxicity to marine organisms, wind speed was increased to 7.5 m/s (shown in Fig. 10). Results show that the predicted toxic areas were larger in the inner parts of the bay (Stations 1 and 2) compared to the mouth of the bay (Stations 3 and 4) regardless of application or non-application of dispersant. Although significantly larger toxic areas were predicted after application of dispersant in Station 4 than non-application, toxic areas were generally smaller compared to the other stations. Moreover, in Station 3 smaller toxic areas were predicted after application of dispersant. While strong wind seems to enhance dispersion of oil in inner sections of the bay that lead to no difference in distribution of oil concentrations between application and non-application of dispersants, the same strong winds seem to facilitate faster natural spreading of chemically-dispersed oil that led to smaller toxic areas after dispersant application. 4. Conclusions Based on the ecotoxicity experiments using diatoms, juveniles of an amphipod and fish embryo of red sea bream, the short-term no-observed effect concentration of oil (EC10 of each experiment) was estimated at 0.01 mg/L. While application of dispersant does not contribute to any toxicity, emulsifying oil by dispersants will increase dissolved oil concentration that can automatically increase the toxic areas around the spilled oil. Moreover, the risk of emulsified and dispersed oil is expected to increase in areas with weaker water current such as in the inner parts of Tokyo Bay. Meanwhile, the risk is expected to decrease in areas with stronger water current such as near the mouth of the bay. Thus, it can be concluded that the level of risk posed by chemically-dispersed oil to marine organisms is similar to non-application of dispersants with regards to the toxic area except when winds are too weak to enhance natural dispersal of spilled oil. References Adams, G.G., Klerks, P.L., Belanger, S.E., Dantin, D., 1999. The effects of the oil dispersant omni-clean on the toxicity of fuel oil No. 2 in two bioassays with the sheepshead minnow Cyprinodon variegates. Chemosphere 39, 2141–2157. Añasco, N.C., Koyama, J., Imai, S., Nakamura, K., 2008. Toxicity of residual chlorines from hypochlorite-treated seawater to marine amphipod Hyale barbicornis and estuarine fish Oryzias javanicus. Water Air Soil Pollut. 195, 129–136. Anderson, J.W., Neff, J.M., Cox, B.A., Tatem, H.E., Hightower, G.M., 1974. Characteristics of dispersants and water–soluble extractions of crude and refined oils and their toxicity to estuarine crustaceans and fish. Mar. Biol. 27, 75–88. Broch, O.J., Slagstad, D., Smit, M., 2013. Modelling produced water dispersion and its direct toxic effects on the production and biomass of the marine copepod Calanus finmarchicus. Mar. Environ. Res. 84, 84–95. Brown, E.D., Norcross, B.L., Short, J.W., 1996. An introduction to studies on the effects of the Exxon Valdez oil spill on early life history stages of Pacific herring, Clupea pallasi, in Prince William sound. Alaska Can. J. Fish. Aquat. Sci. 53, 2337– 2342. Carls, M.G., Rice, S.D., Hose, J.E., 1999. Sensitivity of fish embryos to weathered crude oil: part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval pacifi herring (Clupea pallasi). Environ. Toxicol. Chem. 18, 481–493. Charles, W., Schmidt, M.S., 2010. Between the devil and the deep blue sea: dispersants in the gulf of mexico. Environ. Health Persp. 228 (8), A338–A344.
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Please cite this article in press as: Koyama, J., et al. Simulated distribution and ecotoxicity-based assessment of chemically-dispersed oil in Tokyo Bay. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.04.001