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Effects of organic contaminants on reproduction of the starry flounder Platichthys stellatus in San Francisco Bay

I. Hepatic contamination and mixed-function oxidase (MFO) activity during the reproductive season

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Abstract

Concentrations of neutral organic contaminants and activities of microsomal P-450 mixed-function oxidase (MFO) were measured in the livers of the starry flounder Platichthys stellatus (Pallas), collected from more- and less-contaminated sites in San Francisco Bay, during the 1984–1985 reproductive season. Starry flounder collected at the Berkeley (Bk) site, located in the more urbanized central portion of San Francisco Bay, had greater liver concentrations of polychlorinated biphenyls (PCBs) and polynuclear aromatic hydrocarbons (PAH) (fluorescence equivalents of pyrene) than those collected at a site in northern San Pablo Bay (SP), where urban development is less intense and more distant. Hepatic aryl hydrocarbon hydroxylase (AHH) activity, a particular MFO, in males and in gonadally immature females fluctuated significantly from September 1984 through April 1985 with the Bk population exhibiting significantly greater activities during this period. Site differences were especially notable during the time of spawning (January–March), as AHH activities of starry flounder from SP declined and those from Bk remained elevated. These site differences appear to be due to P-450 isozymes (e.g. P-450E) whose activities are inducible by some PCBs and PAHs, as males and gonadally immature females from the two sites were not different in their hepatic AHH activities when assayed in the presence of an inhibitor of P-450E, 7,8-benzoflavone (7,8-BF). Greatly reduced hepatic AHH activities in females coincided with the onset of vitellogenesis; however, a comparison of female starry flounder bearing yolky eggs from the two sites during several successive reproductive seasons indicated significantly greater AHH activity in those caught at Bk than those from SP. There was a linear relationship between hepatic AHH activity and its inhibition by 7,8-BF in all P. stellatus assayed and more than 98% of individuals caught in San Francisco Bay had hepatic AHH activites that were suppressed by 7,8-BF. Therefore, widespread induction of hepatic microsomal P-450 by PAH-type compounds in San Francisco Bay is indicated and, further, P-450 induction is apparent in female starry flounder in a portion of San Francisco Bay during gametogenesis and the time of spawning.

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Literature cited

  • Colloidi, P., Stekoll, M. S., Rice, S. D. (1984). Hepatic aryl hydrocarbon hydroxylase activities in coho salmon (Oncorhynchus kisutch) exposed to petroleum hydrocarbons. Comp. Biochem. Physiol. 79C: 337–341

    Google Scholar 

  • Chapman, P. M., Dexter, R. N., Cross, S. F., Mitchell, D. G. (1986). A field trial of the sediment quality triad in San Francisco Bay. NOAA natn. mar. Fish. Serv. tech. Memo U.S. Dep. Commerce NOS OMA 25: 1–134

    Google Scholar 

  • DeVlaming, V., Fitzgerald, R., Delahunty, G., Cech, J. J., Jr., Selman, K., Berkeley, M. (1984). Dynamics of oocyte development and related changes in serum estradiol-17β yolk precursor and lipid levels in the teleostean fish, Leptocottus armatus. Comp. Biochem. Physiol. 77A: 599–610

    Google Scholar 

  • Forlin, L., Anderson, T. (1985). Storage conditions of rainbow trout liver cytochrome P-450 and conjugating enzymes. Comp. Biochem. Physiol. 80B: 569–572

    Google Scholar 

  • Forlin, L., Anderson, T., Koivusaari, U. and Hansson, T. (1984) Influence of biological and environmental factors on hepatic steroid and xenobiotic metabolism in fish—interaction with PCB and β-napthoflavone. Mar. envirl Res. 14: 47–58

    Google Scholar 

  • Forlin, L., Haux, C. (1985). Increased excretion in the bile of 17β-[3H]estradiol-derived radioactivity in rainbow trout treated with β-napthoflavone. Aquat. Toxic. 6: 197–208

    Google Scholar 

  • Foureman, G. L., White, N. B., Jr., Bend, J. R.(1983). Biochemical evidence that winter flounder (Pseudopleuronectes americanus) have induced hepatic cytochrome P-450-dependent monoxygenase activities. Can. J. Fish. aquat. Sciences 40: 854–864

    Google Scholar 

  • Freeman, H. C., Sangalang, G., Flemming, B. (1982). The sublethal effects of a polychlorinated biphenyl (Arolor 1254) diet on the Atlantic cod (Gadus morhua). Sci total Envir. 24: 1–11

    Google Scholar 

  • Hansen, P. D., Von Westernhagen, H., Rosenthal, H. (1985). Chlorinated hydrocarbons and hatching success in Baltic herring spring spawners. Mar. envirl Res. 15: 59–76

    Google Scholar 

  • Hansson, T., Gustafson, J.-A. (1981). In vitro metabolism of 4-androstene-3,17-dione by hepatic microsomes from the rainbow trout (Salmo gairdneri): effects of hypophysectomy and estradiol-17β. J. Endocr. 90: 103–112

    Google Scholar 

  • Hartley, P. H. T. (1947). Observations on flounders (Pleuronectes flesus) marked in the estuaries of Tamar and Lynher. J. mar. biol. Ass. U.K. 27: 53–64

    Google Scholar 

  • Klotz, A. V., Stegeman, J. J., Walsh, C. (1983). An aryl hydrocarbon hydroxylating hepatic cytochrome P-450 from the marine fish Stenotomus chrysops. Archs Biochem. Biophys. 226: 578–592

    Google Scholar 

  • Klotz, A. V., Stegeman, J. J., Walsh, C. (1984). Multiple isozymes of hepatic cytochrome P-450 from the marine teleost fish scup (Stenotomus chrysops). Mar. envirl Res. 14: 402–404

    Google Scholar 

  • Lech, J. J., Vodicnik, M. J., Elbcombe, C. R. (1982). Induction of monoxygenase activity in fish. In: Weber, L. J. (ed.) Aquatic toxicology. Raven Press, New York, p. 107–148

    Google Scholar 

  • Lindström-Seppä, P. (1985). Seasonal variation of the xenobiotic metabolizing enzyme activities in the liver of male and female vendace (Coregonus albula L.). Aquat. Toxic. 6: 323–331

    Google Scholar 

  • Little, P. J., James, M. O., Pritchard, J. B., Bend, J. R. (1984). Benzo(a)pyrene metabolism in hepatic microsomes from feral and 3-methylcolanthrene-treated southern flounder, Paralichthys lethostigma. J. envirl Path. Toxic. Oncol. 5: 309–320

    Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951). Protein measurement with the folin phenol reagent. J. biol. Chem. 193: 265–275

    Google Scholar 

  • Mattison, D. R. (1980). Morphology of oocyte and follicle destruction by polycyclic aromatic hydrocarbons in mice. Toxic. appl. Pharmac. 53: 249–259

    Google Scholar 

  • Nebert, D. W., Gelboin, H. U. (1968). Substrate-inducible microsomal aryl hydrocarbon hydroxylase in mammalian cell culture. J. biol. Chem. 243: 6242–6249

    Google Scholar 

  • NOAA (1987) National status and trends program for marine environmental quality. Progress report and preliminary assessment of findings of the benthic survelliance project, 1984. National Oceanic and Atmospheric Administration, Rockville, Md (Ref N/OMA 32)

    Google Scholar 

  • Orcutt, H. G. (1950). The life history of the starry flounder, Platichthys stellatus (Pallas). Calif. Fish Game Bull. 78: 1–64

    Google Scholar 

  • Ozretich, R. J., Schroeder, W. P. (1986). Determination of neutral organic priority pollutants in marine sediment, tissue and reference materials utilizing bonded-phase sorbent. Analyt. Chem. 58: 2041–2047

    Google Scholar 

  • Pantuck, E. J., Pantuck, C. J., Garland, W. A., Min, B., Wattenberg, L. W., Anderson, K. E., Cappas, A., Conney, A. H. (1979). Stimulatory effect of brussel sprouts and cabbage on human drug metabolism. Clin. Pharmac. Ther. 25: 85–88

    Google Scholar 

  • SAS (Statistical Analysis System) (1985). SAS user's guide: statistics. Version 5 ed. SAS, Cary, N. Carolina

    Google Scholar 

  • Selman, K., Wallace, R. A. (1983). Oogenesis in Fundulus heteroclitus. III. Vitellogenesis. J. exp. Zool. 226: 441–457

    Google Scholar 

  • Smith, S. E., Kato, S. (1979). The fisheries of San Francisco Bay: past, present and future. In: Conomos, J. T. (ed.) San Francisco Bay: the urbanized estuary. American Association for the Advancement of Science, San Francisco, p. 445–468

    Google Scholar 

  • Spies, R. B., Felton, J. S., Dillard, L. (1982). Hepatic mixedfunction oxidases in California flatfishes are increased in contaminated environments and by oil and PCB ingestion. Mar. Biol. 70: 117–127

    Google Scholar 

  • Spies, R. B., Rice, D. W., Jr.(1988). Effects of organic contaminants on reproduction of the starry flounder Platichthys stellatus in San Francisco Bay. Part II. Reproductive success of fish captured in San Francisco Bay and spawned in the laboratory. Mar. Biol. 98: 191–200

    Google Scholar 

  • Spies, R. B., Rice, D. W., Jr., Andersen, B. D., Felton, J. S., Diaz, M. (1986). Developmental success and contaminant exposure in Platichthys stellatus from San Francisco Bay. Lawrence Livermore National Laboratory, Rep. No. UCID-19993-85, Livermore, California

  • Spies, R. B., Rice, D. W., Jr., Montagna,P. A., Ireland, R. R. (1985). Reproductive success, xenobiotic contaminants and hepatic mixed function oxidase (MFO) activity in Platichthys stellatus populations from San Francisco Bay. Mar. envirl Res. 17: 117–121

    Google Scholar 

  • Stegeman, J. J., Binder, R. L. (1979). High benzo(a)pyrene hydroxylase activity in the marine fish Stenotomus versicolor. Biochem. Pharmac. 28: 1686–1688

    Google Scholar 

  • Stegeman, J. J., Chevion, M. (1979). Sex differences in cytochrome P-450 and mixed-function oxygenase activity in gonadally-mature trout. Biochem. Pharmac. 29: 553–558

    Google Scholar 

  • Sundararaj, B. I., Wain, P. (1981). Steroid-induced synthesis of vitellogenin in the catfish, Heteropneustes fossilus (Bloch). Gen. comp. Endocr. 43: 201–210

    Google Scholar 

  • Truscott, B., Walsh, J. M., Burton, M. P., Payne, J. F., Idler, D. R. (1983). Effect of acute exposure to crude petroleum on some reproductive hormones in salmon and flounder. Comp. Biochem. Physiol. 75C:121–130

    Google Scholar 

  • Varanasi, U., Gmur, D. J. (1980). Metabolic activation and covalent binding of benzo(a)pyrene to deoxyribonucleic acid catalyzed by liver enzymes of marine fish. Biochem. Pharmac. 29: 753–761

    Google Scholar 

  • Varanasi, U., Gmur, D. J., Treseler, P. A. (1979). Influence of time and mode of exposure on biotransformation of naphthalene by juvenile starry flounder (Platichthys stellatus) and rock sole (Lepidopsetta bilineata). Archs envirl Contam. Toxic. 8: 673–692

    Google Scholar 

  • Varanasi, U., Nishimoto, M., Reichert, W. L., Stein, J. E. (1982). Metabolism and subsequent covalent binding of benzo[a] pyrene to macromolecules in gonads and liver of ripe English sole (Parophrys vetulus). Xenobiotica 12: 417–425

    Google Scholar 

  • Varanasi, U., Stein, J. E., Hom, T. (1981). Covalent binding of benzo(a)pyrene to DNA in fish liver. Biochem. biophys. Res. Commun. 103: 780–787

    Google Scholar 

  • Walton, D. G., Fancey, L. L., Green, J. M., Kiceniuk, J. W., Penrose, W. R. (1983). Seasonal changes in aryl hydrocarbon hydroxylase activity of a marine fish Tautogolabrus adspersus (Walbaum) with and without petroleum exposure. Comp. Biochem. Physiol. 76C: 247–253

    Google Scholar 

  • Wirjoatmodjo, S., Pitcher, T. J. (1984). Flounders follow the tides to feed: evidence from ultrasonic tracking in an estuary. Estuar. cstl Shelf Sci. 19: 231–241

    Google Scholar 

  • Wattenberg, L. W., Loub, W. D., Lam, C. K., Speier, J. L. (1976). Dietary constituents altering responses to chemical carcinogens. Feda Proc. Fedn Am. Socs exp. Biol. 35: 1327–1331

    Google Scholar 

  • Von Westernhagen, H., Rosenthal, H., Dethlefsen, V., Harms, U., Hansen, P. D. (1981). Bioaccumulating substances and reproductive success in Baltic flounder Platichthys flesus. Aquat. Toxic. 1: 85–99

    Google Scholar 

  • Yamamoto, K. (1956). Studies on the formation of fish eggs. I. Annual cycle in the development of ovarian eggs in the flounder, Liopsetta obscure. J. Fac. Sci. Hokkaido Univ. (Ser. 6) 2001. 1 2: 363–373

    Google Scholar 

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Communicated by R. S. Carney, Baton Rouge

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Spies, R.B., Rice, D.W. & Felton, J. Effects of organic contaminants on reproduction of the starry flounder Platichthys stellatus in San Francisco Bay. Mar. Biol. 98, 181–189 (1988). https://doi.org/10.1007/BF00391193

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