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Primary and secondary stress responses of striped bass (Morone saxatilis) exposed to benzene

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Abstract

Striped bass (Morone saxatilis) were collected from the San Francisco Bay-Delta estuary in 1982, from areas distant from pollution sources. After acclimatization, plasma cortisol concentration (primary response) and blood biochemicals indicative of energy mobilization (secondary responses) were followed in individuals exposed to sublethal levels of benzene for up to 21 d. Despite the persistence of benzene in blood and liver tissues for the exposure duration, stress responses were moderate and returned to control values within the initial 7 d. Blood and liver rapidly accumulated benzene to approximately 20 times the exposure concentrations (0.1 and 1.0 ppm). Concentrations of cortisol and secondary response variables were not proportional to benzene exposure or to accumulation levels, however. Plasma cortisol concentrations increased two- to three-fold at 8 h and returned to control levels prior to 48 h exposure. Glucose, lactate, H+, protein and triglyceride concentrations were elevated during the initial 4 h to 7 d, with protein and triglyceride returning to normal levels prior to the other secondary response variables. From the perspective of the general adaptation syndrome (GAS), benzene activated the hypothalamo-pituitary-interrenal axis, resulting in clinical stress responses characteristics of an alarm reaction. The time-courses and amplitudes of primary and secondary responses to benzene suggest the sensory perception of a noxious agent eliciting mild, acute stress followed by adaptation.

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Literature cited

  • Anderson, J. W., J. M. Neff, B. A. Cox, H. E. Tatem and G. M. Hightower: Characteristics of dispersions and water-soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish. Mar. Biol. 27, 75–88 (1974)

    Google Scholar 

  • Babcock, M. M.: Morphology of olfactory epithelium of pink salmon, Oncorhynchus gorbuscha, and changes following exposure to benzene: a scanning electron microscopy study. In: Marine biology of polar regions and effects of stress on marine organisms, Ed. by J. S. Gray and M. E. Christiansen. London: John Wiley and Sons (In press)

  • Barton, B. A., R. E. Peter and C. R. Paulencu: Plasma cortisol levels of fingerling rainbow trout (Salmo gairdneri) at rest, and subjected to handling, confinement, transport, and stocking. Can. J. Fish. aquat. Sciences 37, 805–811 (1980)

    Google Scholar 

  • Benville, P. E., Jr. and S. Korn: The acute toxicity of six monocyclic aromatic crude oil components to striped bass (Morone saxatilis) and bay shrimp (Crago franciscorum). Calif. Fish Game 63, 204–209 (1977)

    Google Scholar 

  • Benville, P. E., Jr., T. G. Yocom, P. Nunes and J. M. O'Neill: Simple, continuous-flow systems for dissolving the water-soluble components of crude oil into seawater for acute or chronic exposure of marine organisms. Wat. Res. 15, 1197–1204 (1981)

    Google Scholar 

  • Black, E. C.: Hyperactivity as a lethal factor in fish. J. Fish. Res. Bd Can. 15, 573–586 (1958)

    Google Scholar 

  • Black, E. C., W. J. Chin, F. D. Forbes and A. Hanslip: Changes in pH, carbonate, and lactate of the blood of yearling Kamloops trout, Salmo gairdneri, during and following severe muscular activity. J. Fish. Res. Bd Can. 16, 391–402 (1959)

    Google Scholar 

  • Bondy, P. K.: The adrenal cortex. In: Metabolic control and disease, 8th ed. pp 1427–1500. Ed. by P. K. Bondy and L. E. Rosenberg. Philadelphia: W. B. Saunders Co. 1980

    Google Scholar 

  • Bouck, G. R.: Effects of diurnal hypoxia on electrophoretic protein fractions and other health parameters of rock bass (Amblophites rupestris). Trans. Am. Fish. Soc. 101, 488–493 (1972)

    Google Scholar 

  • Brocksen, R. W. and H. T. Bailey: Respiratory response of juvenile chinook salmon and striped bass exposed to benzene, a water-soluble component of crude oil. In: Proceedings of a Joint Conference on Prevention and Control of Oil Spills, pp 783–791. Washington, D.C.: American Petroleum Institute 1973

    Google Scholar 

  • Brown, S. B., J. G. Eales, R. E. Evans and T. J. Hara: Interrenal, thyroidal, and carbohydrate responses of rainbow trout (Salmo gairdneri) to environmental acidification. Can. J. Fish. aquat. Sciences 41, 36–45 (1984)

    Google Scholar 

  • Bucolo, G. and H. David: Quantitative determinations of serum triglycerides by the use of enzymes. Clin. Chem. 19, 476–482 (1973)

    Google Scholar 

  • Cliff, G. and G. D. Thurman: Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp. Biochem. Physiol. 78A, 167–173 (1984)

    Google Scholar 

  • Conney, A. H.: Pharmacological implications of microsomal enzyme induction. Pharmac. Rev. 19, 317–366 (1967)

    Google Scholar 

  • Cornish, H. H.: Solvents and vapors. In: Toxicology: the basic science of poisons, 2nd ed. pp 468–496. Ed. by J. Doull, C. D. Klaassen and M. O. Amdur. New York: Macmillan 1980

    Google Scholar 

  • Delahunty, G., J. Olcese, M. Prack, M. J. Vodicnik, C. B. Schreck and V. DeVlaming: Diurnal variations in the physiology of the goldfish, Carassius auratus. J. interdiscip. Cycle Res. 9, 73–88 (1978)

    Google Scholar 

  • DiMichele, L. and M. H. Taylor: Histopathological and physiological responses of Fundulus heteroclitus to naphthalene exposure. J. Fish. Res. Bd Can. 35, 1060–1066 (1978)

    Google Scholar 

  • Donaldson, E. M.: The pituitary-interrenal axis as an indicator of stress in fish. In: Fish and stress, pp 11–48. Ed. by A. D. Pickering. London: Academic Press 1981

    Google Scholar 

  • Donaldson, E. M. and H. M. Dye: Corticosteroid concentrations in sockeye salmon (Oncorhynchus nerka) exposed to low concentrations of copper. J. Fish. Res. Bd Can. 32, 533–539 (1975)

    Google Scholar 

  • Duncan, D. B.: Multiple range and multiple F tests. Biometrics 11, 1–42 (1955)

    Google Scholar 

  • Gadbois, D. F. and R. S. Maney: Survey of polychlorinated biphenyls in selected finfish species from United States coastal waters. Fish. Bull. U.S. 81, 389–396 (1983)

    Google Scholar 

  • Gerarde, H. W.: Toxicology and biochemistry of aromatic hydrocarbons, 329 pp. New York: Elsevier 1960

    Google Scholar 

  • Grant, B. F. and P. M. Mehrle: Endrin toxicosis in rainbow trout (Salmo gairdneri). J. Fish. Res. Bd Can. 30, 31–40 (1973)

    Google Scholar 

  • Hanes, D., H. Krueger, I. Tinsley and C. Bond: Influence of pentachlorophenol on fatty acids of coho salmon. Proc. west. Pharmac. Soc. (U.S.) 11, 121–125 (1968)

    Google Scholar 

  • Hirsch, N. D., J. A. Whipple and P. E. Benville, Jr.: Introduction of monocyclic aromatics into seawater by an outboard motor. Envirl Monitg Assessmt (In press)

  • Holmberg, B., S. Jensen, A. Larsson, K. Lewander and M. Olsson: Metabolic effects of technical pentachlorophenol (PCP) on the eel Anguilla anguilla L. Comp. Biochem. Physiol. 43B, 171–183 (1972)

    Google Scholar 

  • Hughes, G. M.: Effects of low oxygen and pollution on the respiratory systems of fish. In: Fish and stress, pp 121–146. Ed. by A. D. Pickering. London: Academic Press 1981

    Google Scholar 

  • Jerina, D. M. and J. M. Daly: Arene oxides: a new aspect of drug metabolism. Science, N.Y. 185, 573–582 (1974)

    Google Scholar 

  • Kelley, D. W.: The striped bass decline in the San Francisco Bay-Delta estuary, 58 pp. Sacramento, Calif.: California State Water Resources Control Board 1982

    Google Scholar 

  • Korn, S., N. Hirsch and J. W. Struhsaker: Uptake, distribution and depuration of 14C-benzene in northern anchovy, Engraulis mordax, and striped bass, Morone saxatilis. Fish. Bull. U.S. 74, 545–551 (1976)

    Google Scholar 

  • Korn, S., N. Hirsch and J. W. Struhsaker: The uptake, distribution and depuration of 14C-benzene and 14C-toluene in Pacific herring, Clupea harengus pallasi. Fish. Bull. U.S. 75, 633–636 (1977)

    Google Scholar 

  • Kupfer, D.: Effects of pesticides and related compounds on steroid metabolism and function. CRC critical Rev. Toxic. 4, 83–124 (1975)

    Google Scholar 

  • Kupfer, D. and L. Peets: The effect of o, p'DDD on cortisol and hexabarbitol metabolism. Biochem. Pharmac. 15, 573–581 (1966)

    Google Scholar 

  • Leach, G. J. and M. H. Taylor: The role of cortisol in stress-induced metabolic changes in Fundulus heteroclitus. Gen. comp. Endocr. 42, 219–227 (1980)

    Google Scholar 

  • Lee, R. F., R. Sauerheber and G. H. Dobbs: Uptake, metabolism and discharge of polycyclic aromatic hydrocarbons by marine fish. Mar. Biol. 17, 201–208 (1972)

    Google Scholar 

  • Love, R. M.: The chemical biology of fishes, Vol. 2. 943 pp. London: Academic Press 1980

    Google Scholar 

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

    Google Scholar 

  • MacFarlane, R. B.: Determination of corticosteroids in fish plasma by high performance liquid chromotography: evaluation of the method using striped bass (Morone saxatilis). Can. J. Fish. aquat. Sciences 41, 1280–1286 (1984)

    Google Scholar 

  • Mazeaud, M. M. and F. Mazeaud: Adrenergic responses to stress in fish. In: Fish and stress, pp 49–75. Ed. by A. D. Pickering. London: Academic Press 1981

    Google Scholar 

  • Mazeaud, M. M., F. Mazeaud and E. M. Donaldson: Primary and secondary effects of stress in fish: some new data with a general review. Trans. Am. Fish. Soc. 106, 201–212 (1977)

    Google Scholar 

  • Meyerhoff, R. D.: Acute toxicity of benzene, a component of crude oil, to juvenile striped bass (Morone saxatilis). J. Fish. Res. Bd Can. 32, 1864–1866 (1975)

    Google Scholar 

  • Moser, M., J. A. Sakanari, C. A. Reilly and J. Whipple: Prevalence, intensity, longevity and persistence of Anasakis sp. larvae and Lacistorhynchus tenuis metacestodes in San Francisco striped bass. NOAA natn. mar. Fish. Serv. Tech. Rep. U.S. Dep. Commerce 29, 1–4 (1985)

    Google Scholar 

  • Nie, N. H., C. H. Hull, J. G. Jenkins, K. Steinbrenner and D. H. Bent: Statistical package for the social sciences, 2nd ed. New York: McGraw-Hill, Inc. 1975

    Google Scholar 

  • Nowicki, H. C. and A. W. Norman: Enhanced hepatic metabolism of testosterone, 4-androstene-3,17-dione, and estradiol-17β in chickens pretreated with DDT or PCB. Steroids (Oakland, Calif.) 19, 85–93 (1972)

    Google Scholar 

  • Peters, G., H. Delventhal and H. Klinger: Physiological and morphological effects of social stress in the eel (Anguilla anguilla L.). Arch. Fisch Wiss. 30, 157–180 (1980)

    Google Scholar 

  • Pickering, A. D., T. G. Pottinger, and P. Christie: Recovery of brown trout, Salmo trutta L., from acute handling stress: a time-course study. J. Fish Biol. 20, 229–244 (1982)

    Google Scholar 

  • Roubal, W. T., T. K. Collier and D. C. Malins: Accumulation and metabolism of carbon-14 labeled benzene, naphthalene, and anthracene by young coho salmon (Oncorhynchus kisutch). Archs envir. Contam. Toxic. 5, 513–529 (1977)

    Google Scholar 

  • Schreck, C. B.: Stress and compensation in teleostean fishes: response to social and physical factors. In: Fish and stress, pp 295–321. Ed. by A. D. Pickering. London: AcademicPress 1981

    Google Scholar 

  • Schreck, C. B. and H. W. Lorz: Stress response of coho salmon (Oncorhynchus kisutch) elicited by cadmium and copper and potential use of cortisol as an indicator of stress. J. Fish. Res. Bd Can. 35, 1124–1129 (1978)

    Google Scholar 

  • Selye, H.: Stress and the general adaptation syndrome. Br. med. J. 1, 1383–1392 (1950)

    Google Scholar 

  • Silver, R. H. and C. C. Porter: Nitrogen balance, liver protein repletion and body composition of cortisone treated rats. Endocrinology 52, 518–525 (1953)

    Google Scholar 

  • Silbergeld, E. K.: Blood glucose: a sensitive indicator of environmental stress in fish. Bull. envir. Contam. Toxic. 11, 20–25 (1974)

    Google Scholar 

  • Sivarajah, K., C. S. Franklin and W. P. Williams: The effects of polychlorinated biphenyls on plasma steroid levels and hepatic microsomal enzymes in fish. J. Fish Biol. 13, 401–409 (1978)

    Google Scholar 

  • Snyder, R. and J. J. Kocsis: Current concepts of chronic benzene toxicity. CRC critical Rev. Toxic. 4, 265–288 (1975)

    Google Scholar 

  • Stevens, D. E., D. W. Kohlhorst and L. W. Miller: The decline of the striped bass in the Sacramento-San Joaquin estuary, CA. Trans. Am. Fish. Soc. 114, 12–30 (1985)

    Google Scholar 

  • Thomas, P. and J. M. Neff: Plasma corticosteroid and glucose responses to pollutants in striped mullet: different effects of naphthalene, benzo (a) pyrene and cadmium exposure. In: Marine pollution and physiology: recent advances, pp 63–82. Ed. by F. J. Vernberg, A. Calabrese, F. P. Thurberg and W. B. Vernberg. New York: Academic Press 1985

    Google Scholar 

  • Thomas, P., H. W. Wofford and J. M. Neff: Biochemical stress responses of striped mullet (Mugil cephalus L.) to fluorene analogs. Aquat. Toxic. 1, 329–342 (1981)

    Google Scholar 

  • Thomas, P. B. R. Woodin and J. M. Neff: Biochemical responses of the striped mullet Mugil cephalus to oil exposure. I. Acute responses — interrenal activation and secondary stress responses. Mar. Biol. 59, 141–149 (1980)

    Google Scholar 

  • Tomasso, J. R., K. B. Davis and B. A. Simco: Plasma corticosteroid dynamics in channel catfish (Ictalurus punctatus) exposed to ammonia and nitrite. Can. J. Fish. aquat. Sciences 38, 1106–1112 (1981)

    Google Scholar 

  • Walton, M. J. and C. B. Cowey: Aspects of intermediary metabolism in salmonid fish. Comp. Biochem. Physiol. 73B, 59–79 (1982)

    Google Scholar 

  • Wardle, C. S.: Non-release of lactic acid from anaerobic swimming muscle of plaice Pleuronectes platessa L.: a stress reaction. J. exp. Biol. 77, 141–155 (1978)

    Google Scholar 

  • Wedemeyer, G. A. and D. J. McLeay: Methods for determining the tolerance of fishes to environmental stressors. In: Fish and stress, pp 247–275. Ed. by A. D. Pickering. London: Academic Press 1981

    Google Scholar 

  • Whipple, J. A., D. G. Crosby and M. Jung: Third progress report: cooperative striped bass study, 208 pp. Sacramento, California: California State Water Resources Control Board 1983. (Toxic Substances Control Program, Special Projects Report No. 83-3 sp)

    Google Scholar 

  • Whipple, J. A., M. B. Eldridge and P. E. Benville, Jr.: An ecological perspective of the effects of monocyclic aromatic hydrocarbons on fishes. In: Biological monitoring of marine pollutants, pp 483–551. Ed. by F. J. Vernberg, A. Calabrese, F. P. Thurberg and W. B. Vernberg. New York: Academic Press 1981

    Google Scholar 

  • Whipple, J. A., M. Jung, R. B. MacFarlane and R. Fischer: Histopathological manual for monitoring health of striped bass in relation to pollutant burdens. NOAA natn. mar. Fish. Serv. tech. Memo U.S. Dep. Commerce SWFC 46, 1–81 (1984)

    Google Scholar 

  • Whipple, J. A., T. G. Yocom, P. E. Benville, Jr., D. R. Smart, M. H. Cohen and M. E. Ture: Transport, retention and effects of the water-soluble fraction of Cook Inlet crude oil in experimental food chains. In: Marine biological effects of OCS petroleum development, pp 106–129. Ed. by D. A. Wolfe. Boulder, Colorado: National Oceanic and Atmospheric Administration 1978. (Tech. Memo. ERL OCSEAP-1)

    Google Scholar 

  • Wood, C. M., B. R. McMahon and D. G. McDonald: An analysis of changes in blood pH following exhausting activity in the starry flounder, Platichthys stellatus. J. exp. Biol. 69, 173–185 (1977)

    Google Scholar 

  • Wood, C. M., J. D. Turner and M. S. Graham: Why do fish die after severe exercise? J. Fish Biol. 22, 189–201 (1983)

    Google Scholar 

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Communicated by R. S. Carney, Moss Landing

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MacFarlane, R.B., Benville, P.E. Primary and secondary stress responses of striped bass (Morone saxatilis) exposed to benzene. Marine Biology 92, 245–254 (1986). https://doi.org/10.1007/BF00392842

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