A study of the toxicity of Kuwait Crude Oil to the copepod Tigriopus californicus (Baker, 1912). Robert Dorit Hopkins Marine Station Biology 175 H Spring, 197 ABSTRACT The toxicity of several preparations obtained from Kuwait Crude oil to Tigriopus californicus was investigated. Whole oil, sea water extracted whole oil, the seawater extract, and similar materials obtained from oil weathered for 40 days were compared. The LDg's may be ranked as follows; The most toxic preparation was the seawater extract, followed by Whole Kuwait oil, washed Kuwait oil, weathered oil and washed weathered oil, in order of decreasing toxicity. Males were found to be twice as susceptible as females to the whole oil preparation. Assays conducted in an attempted simulation of the tidepool environment revealed higher toxicities than were cbtained under more traditional methods of assay. INTRODUCTION A considerable body of information dealing with both field and laboratory toxicity of oil and petroleum products to marine organisms has been generated in the last decade (see Moore, 1973). Most of this work has tended to focus on economically important species such as oysters or clams. Until recently, little was known about the impact of oil pollution on representative copepods. Mironov (1968, 1969) examined the response of Black Sea copepods to crude cil, and reports impact of 1.0 ppm of crude oil on the survival of copepods. More recent work by Kontgiannis and Barnett (1973,1975) studied the toxicity of crude oil and crude oil fractions on Tigriopus californicus, concluding that effects were due to both the blocking of oxygen transport across the air-water interface and to toxic materials present in the oil. The present study attempts to examine the toxic effect of Kuwait Crude oil on a high tidepool organism, Tigriopus californicus. Whole fresh oil as well as weathered oil were compared for toxicity. Sea water soluble and less sea water soluble fractions of these materials were also studied. An attempt at a closer simulation of tidepool conditions in toxicity tests is presented, as well as an investigation of differential susceptibility of males and females in the copepod population. METHODS AND MATERIALS T. californicus used in this study were collected from a high tidepool located at Mussel Point in Pacific Grove, California. Animals were kept in two large bowls of filtered seawater at room temperature. Water was changed every two days. The diet supplied to the animals was Tetramin fish food (Telia Werke, West Germany). Prior to any experiment, a rundown sample of T. californicus was taken from the aquarium and placed under a dissecting scope for removal of copulating pairs and larvae, along with dead and moribund specimens. Ten animals were subjected to each dose of the test materials. The fractions of oil used in this study are all derived from an original one gallon sample of American Petroleum Institute Reference Kuwait Crude, referred to in this paper as Whole Kuwait. This sample was generously pro¬ vided by Dr. John Martin of Moss Landing Marine Laboratory in Moss Landing, California. The Washed Kuwait fraction was prepared by mixing one part of Whole Kuwait with three parts of fresh filtered seawater. The mixing was done manually in a separating funnel by shaking vigorously for five minutes. Separation was then allowed to proceed for approximately 90 minutes before water was drained from the funnel. The process was repeated five times with fresh filtered seawater. The water extracted after the fifth wash showed no toxicity to Tigriopus c. over a 96 hour test period. The soluble fraction of Kuwait Crude oil was obtained by extracting one part of oil with two parts of seawater in a separating funnel, mixed vigorously by hand for five minutes. The mixture was allowed to stand for two hours and was then mixed again. This process was repeated a third time, The mixture was then allowed to separate for approximately 12 hours before the water was removed and filtered through Whatman l filter paper (Whatman Manufacturers, England) to remove any microparticles of oil that might have remained in suspension. This soluble fraction was tested immediately after preparation. The weathered oil was prepared by placing 100 ml. of Whole Kuwait cil with 400 ml. of seawater in a large beaker that was then placed outdoors, in full sunlight for 40 days. The residue was more viscous than the original oil. Water was removed from the beaker as completely as was possible. The washed weathered oil was obtained using the washing procedure described above. With the exception of the soluble fraction (administered by volume). all other fractions were administered by weight and carefully placed on the surface of the sea water containing the test animals. All tests were carried out in 30 ml. glass stoppered bottles, with a final water volume of 25 ml. Animals were examined at regular intervals to record the number of deaths, Any animal that did not respond to shaking was considered dead. Oxygen determinations were carried out using the Winkler technique (Strickland and Parsons, 1965). The results of toxicity titrationswere analyzed using the approximate probit method of Litchfield and Wilcoxon (Litchfield and Wilcoxon, 1949). This method provides a factor f LD.. The product and quotient of this factor with the LD yields 958 confidence limits for the LD5. Potency ratios, P.R., may be obtained as a comparison between toxicants. The factor Ipg must be less than P.R. for there to be a significant difference between EDgo's. Generally, log-dose effect plots were drawn using the results of two independent toxicity titrations.The assays were terminated when no further mortality was noted. In all cases, control mortalities over the prescribed time period, h dawe wene zero RESULTS Figures 1,2,3,4 and 5 show the lethal effect of various fractions for Tigriopus californicus. Dose is shown in grams/liter of water vs. 9 mortality. Table 1 summarizes the information obtained from the previous plots. The LDgo's, along with their 95 confidence limits show the varying toxicities of the different fractions. Table 1 shows that the different fraction used in this study exhibit different toxicities for T. californicus. Apparent differences in the toxicity of the fractions point to the necessity of a careful definition of the history of the oil when describing its toxicity. The soluble fraction, a seawater extract of the most water soluble components of Kuwait Crude oil shows the highest toxicity to the copepod T. californicus. It should be mentioned that the volume of soluble fraction that was administered to the copepods was translated into a weight dose by using Anderson's estimate of the solubility of Kuwait Crude oil in seawater (Anderson, et al, 1974). Although the technique used here differs substantially from the one described by Anderson, the figure of 21.68 ppm of oil in solution was considered the best available estimate of the solubility of this oil in sea¬ water. Where the toxicant formed a surface film, oxygen determinations were carried out at the end of the assays, showing no noticeable decrease in the dissolved oxygen in experimental vessels; except a decrease to 40% of saturation at the high doses of washed oil. Oxygen levels of as little as 203 saturation have been found to have little effect in survival of T. californicus (Fahey, 1977). Table 2 compares the toxicities of several different fractions using the potency ratio as a quantitative measure. The factor fpp and the 95% confidence limits for Potency Ratios are also presented. The potency ratio of Whole Kuwait vs. Washed Kuwait is a measure of the important loss of toxicity that occurs upon removal of the seawater soluble fraction. The weathering of crude oil results in an almost seven fold reduction in its toxicity to T. californicus. The potency ratio of Washed Kuwait vs. weathered oil indicates that weathering is the more effective mechanism for the reduction of toxic constituents. Subsequent washing of the weathered oil does not yield a significantly less toxic material. A comparison of the susceptibility of adult male and female T. californicus to Whole Kuwait Crude oil yielded the results presented in figure 6. Females with external egg masses were excluded from the female test population. The LDgo for females was .195 grams/liter, with 95% confidence limits of .123 and .309. The LDg for males was .092 grams/liter with 95 confidence limits of .Obl and .139. A comparison provided a potency ratio of 2.12 and an fpp of 1.84, indicating a significant difference in the susceptibility of the sexes. Females with internal eggs in darkened ovaries were observed to survive 2-3 days longer than females with external egg masses or females with empty ovaries. A closer simulation of high tidepool conditions was attempted by con¬ ducting the toxicity titrations in the presence of sand and naturally occuring drift algae. Approximately 7.5 mm. of washed sand were used to cover approximately 2 grams of fresh Macrocystis pyrifera in the bottcm of assay bottles. Washed oil was added and the toxicity compared to that obtained in assays lacking sand and algae. Figure 7 presents the results. The toxicity was greater under the simulating conditions. Without sand and algae, the LD was .405 grams/liter with 958 confidence limits of .252 and .650. In the simulations the LD was .080 grams/liter with 958 confidence limits A comparison gave a potency ratio of 5.06 and an fy of .051 and .12 of 1.89, indicating a significant potency difference in the two conditions. Oxygen levels in both controls and experimental bottles were less than 10% of saturation when the assay was terminated. There were no mortalities in the controls as the animals managed to obtain oxygen by hovering near the surface. Although animals behaved similarly in the bottles containing oil, the oil film may have inhibited respiration at the surface. The degree to which this enhancement of oil toxicity is due to interference with oxygen diffusion is difficult to evaluate. The aqueous phase removed from the assays was tested and proved not to be toxic to T. californicus after a period of aeration. DISCUSSION It is known that the most soluble components of crude oil are the short chain alkanes and light aromatics (Anderson, et al, 1974) Consequently it appears that these seawater soluble compounds are highly toxic to T. californicus. The steeper slope of the dose effect curve of the soluble fraction may be an indication of the acute toxicity of the preparation. Immediate sublethal effects include a marked decrease in the activity of T. californicus. The narcotic effect of crude oil, in particular of the soluble fraction has been mentioned before (Goldacre, 1968). Other workers have identified soluble material as the acutely toxic fraction of oil, with benzenes and napthalenes being singled out as particularly toxic to marine invertebrates (Anderson, 1974; Blumer, 1970; Boylan, 1971; Ottaway, 1971; Shelton, 1971). It is probable that the large dilution volumes present in the open ocean, combined with the relatively low solubility of these hydrocarbon compounds may result in negligible concentrations of soluble aromatics other organics in the ocean. The situation in the high tidepool, however, may be considerably more critical, given that the smaller volumes of water available for dilution may enable the levels of solubilized hydrocarbons in the water column to reach lethal concentrations. Whole Kuwait also exhibited considerable toxicity to T. californicus. This whole oil is the source of the soluble hydrocarbons accounting for the toxicity of the soluble fraction. However, the rate of diffusion of aromatics and short chain saturates from a surface layer of oil is probably relatively slow and results in low concentrations of solubilized hydrocarbons. The uptake by T. californicus of any of the soluble components may result in further release of substances from the oil film. Washed Kuwait, although treated in a manner that removes all or most of the readily soluble materials from crude oil, nevertheless exhibits toxicity to T. californicus and probably indicates residual toxic materials not removed by the wash procedure. In attempting to ascertain the reasons for the toxicity of Whole weathered oil, it should be kept in mind that the same short chain alkanes and light aromatics that are seawater soluble are the most volatile hydrocarbons present (Lockwood, 1976). The 40 day weathering period left a residue that has been altered by volatilization, dissolution, microbial action and autooxidation (Moore,1973 ; Butler, 1974). The first two processes, volatilization and dissolution,remove the fraction of oil with boiling points below. 250° C, probably within a matter of hours (Moore, 1973). Further loss of toxicity may result from the shortening of certain alkane chains by auto¬ oxidation or microbial action, and consequently increase solubility and volatility. In addition to the differential susceptibility of males and females to Kuwait Crude oil, it was noted that among the females, those with darkened ovaries and oviducts,indicating the presence of ripe eggs but preceeding the laying of the eggs, survived as long as 2 or 3 days more than females with external egg masses or empty ovaries. Perhaps at least some of the lipid soluble toxicants are deposited in the developing eggs, resulting iu a decrease in the internal effective concentration of these toxicants in the particular female. An investigation of the viability of larval forms born to these females should prove interesting as a subject for further investigation. Coroner noted a decrease in clutch size in the copepod Eurytemora affinis following exposure to oil (Coroner, 1975). Therefore, there may be further effects on fertility. The attempts at simulation of some tidepool conditions in toxicity titrations illustrate some of the deficiencies of the usual laboratory assays as measures of toxicity in the natural environment. Other effects, such as a decrease in photosynthetic efficiency in tidepools where surface is coated with oil may result in further deleterious effects. Although a fresh spill occuring near the shore seems to pose the most immediate threat to the high tidepool environment and its inhabitants, the effect of washed, weathered oil on Tigriopus californicus remains far from negligible. ACKNOVLEDGEMENT I would like to extend my appreciation to the faculty and students of the 175H class at Hopkins Marine station, and in particular to Dr. John Phillips whose editing and suggestions were enormously useful. Thanks also to Moss Landing Marine Labs for the sample of Kuwait Crude oil. Finally, a special word of thanks to Gillian Kendall, without whom this quarter would not have been quite the same. BIBLIOGRAPHY harateristics of dispersions and water Anderson, J.W., et al. (1974). soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish. Marine Biology, 27, 75-88. C.J., Kontogiannis, J.E. (1975). The effect of crude oil fractions Barnett. on the survival of a tidepool copepod, T. californicus. Environmental Pollution, 8, 45-54 M., et al. (1970). Hydrocarbon pollution of edible shellfish by oil Blumer, spill. Marine Biology, 5, 195-202. D.B., Tripp, B.W.(1971). Determination of hydrocarbons in seawater Boylan extracts of crude oil and crude oil fractions, Nature, 230, 44-47. Butler, M.J.A., et al. (1974). Biological aspects of oil pollution in the marine environment - a review. MSC Report, 22A. E.D.S. (1975). Fate of fossil fuel hydrocarbons in marine animals. Coroner, Proc. R. Soc. Lond., B. 189, 391-413. (1977). Some adaptations to anaerobiasis in T. californicus. Biology Fahey, M., 175 H, Hopkins Marine Station. Goldacre, R.J. (1968). The effects of detergents and oils on the cell membrane, in The biological effects of oil pollution on littoral communities, Carthy, 0.D. and Arthur, D.R., eds., Field Studies Council. 131-138. Kiontogiannis, J.E., Barnett, C.J. (1973). The effect of oil pollution on survival of the tidal pool copepod, T. californicus. Environmental Pollution, 4, 69-79. Litchfield, J.T., Wilcoxon, F. (1949). A simplified method of evaluating dose-effect experiments. J. of Pharmacology, 96, 99-113. Lockwood, A.P.M. (1976). Effects of pollutants on aquatic organisms, Cambridge University Press, London. O.G. (1968) Hydrocarbon pollution of the sea and its influence Mironoy on microorganisms. Helgolander Wiss. Meersunters, 17, 335-339. O.G., (1969). Effect of oil pollution upon some representatives Mironoy, of Black Sea zooplanktcn. Zoologicheskii Zhurnal, 48, 980-984. Moore, S.F., et al. (1973). A preliminary assessment of the envirormental vulnerability of Machias Bay, Maine to oil supertankers. Report No. MITSG 73-6, Sea Grant. S. (1971), The comparative toxicities of crude oils in The ecological Ottaway, effects of oil pollution on littoral communiries, E.B. Cowell, ed. Institute of Petroleum, 172-180. R.G.J. (1971). Effects of oil and oil dispersants on the marine Shelton, environment, Proc. Roy. Soc. Lond. B., 177, 411-422. Strickland,J.p., Parsons, T.R. (1965). Handbook of seawater analysis Fisheries research board of Canada, Bulletin No. 125. Figure 1. Log Dose vs. Percent Mortality of Whole Kuwait Crude Oil, Each point represents the percent mortality observed using 10 T. californicus. Two separate assays were used in obtaining the line and are distinguished by open and closed circles. The LD is 130 grams/liter with 958 confidence limits of .092 and .184. 1o MORTALITY 991 95 90 80 70 60 50 40 30 20 10 5 -- 0 .03 .04 A .20 — .50 900 kk - .10 — Figure 2. Log Dose vs. Percent Mortality of Washed Kuwait Crude Oil. Each point represents the percent mortality observed using 10 T. call fornicus. Two separate assays were used in obtaining the line and are distinguished by opened and closed circles. The LDg is .405 grams/liter with 958 confidence limits of .252 and .650. 2 k k- staatatakakava- L Figure 3. Log Dose vs. Percent Mortality of The Soluble Fraction. Each point rep ents percent mortality observed using 10 T. californicus, Two separate assays were used in obtaining the line and are distinguished by open and closed circles. The LDg is .008 grams/liter with 953 confidence limits of .007 and.009. 1o MORTALITY 99 95 90 80 70 60 50 40 30 20 101 o0 . . .. 0 .003 — .005 — .02 — .05 Figure 4. Log Dose vs. Percent Mortality of Weathered Oil. Each point represents the percent mortality observed using 10 T. californicus. Two separate assays were used in obtaining the line and are distinguished by open and closed circles. The LD is.900 grams/liter with 95% confidence limits of .550 and 1.434. 2 — aataaaaaata- S Figure 5. Log Dose vs. Percent Mortality of Washed Weathered Oil. Each point represents the percent mortality observed using 10 T. californicus. Two separate assays were used in obtaining the line and are distinguished by open and closed circles. The LDg is 3.001 grams/liter with 958 confidence limits of .911 and 9.886. O 2 3 kataatatatatavaa- 1 S L TABLE 1 COMPARISON OF EDgO'S FOR VARIOUS FRACTIONS OF KUWAIT CRUDE OIL f EDg 958 LIMITS E0 1.1234 SOLUBLE .0086 g/1 .0076 g/1 FRACTION .0068 g/1 1.4178 .184 g/1 WHOLE .130 g/1 .092 g/1 KUWAIT 1.6506 .650 g/1 WASHED .405 g/1 .252 g/1 KUWAIT 1.6374 1.474 g/1 .900 g/1 WHOLE .550 g/1 WEATHERED OIL 9.886 g/1 3.2945 3.001 g/1 WASHED .911 g/1 WEATHERED OIL TABLE 2 POTENCY RATIOS OF VARIOUS FRACTIONS OF KUWAIT CRUDE OIL 958 LIMIT P.R. 5.545 WHOLE KUWAIT/ 1.78 3.115 WASHED KUWAIT 1.750 6.923 12.599 WHOLE KUWAIT/ 1.82 3.804 WEATHERED OIL WASHED KUWAIT/ 4.377 1.97 2.222 WEATHERED OIL 1.128 WEATHERED OIL/ NOT SIGNIFICANT TO P=.05 WASHED WEATHERED OIL — Figure 6. Comparison of the susceptibilities of male and female adults of the species Tigriopus californicus to whole Kuwait Crude Oil. Open and closed squares represent two separate assays performed on male T. californicus and yield an LD of .092 grams/liter with 95% confidence limits of .139 and .061. Open and closed squares represent two separate toxicity assays using female T. californicus. LD for females is .195 grams/liter, with 95% confidence limits of .309 and .123. a 2 ktaaaaataata- Figure 7. Comparison of the Log Dose vs. Percent Mortality plots of washed Kuwait Crude Oil to T. californicus as assayed in a simulated tidepool condition containing algae and sand,and containing only seawater. Open and closed circles represent two separate assays in only seawater. Squares represent toxicity titration performed in a simulated tidepool situation. The LD for washed Kuwait Oil assayed in seawater is.405 grams/liter, with 95% confidence limits of .650 and .252. The LD., obtained in the tidepool simulation is .080 grams/liter, with 958 confidence limits of .125 and .051. 7o MORTALITY 991 95 90f 804 701 60 50 40 30 20 10 6 0 a o .03 .04 kt- 10 20 50 — 0