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Hydrocarbon bioaccumulation from contaminated sediment by the deposit-feeding polychaeteAbarenicola pacifica

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Abstract

This study examines the role of the organic carbon content of sediment in aromatic hydrocarbon bioaccumulation and assesses the importance of two routes of hydrocarbon uptake: (1) the uptake of the particulate contaminant fraction from ingested sediment; (2) the uptake of the dissolved contaminant fraction from interstitial or overlying water. The lugwormAbarenicola pacifica was collected from San Juan Island, Washington, USA, in January 1989, and exposed to three sediments contaminated with [3H]benzo (a) pyrene (BaP). By manipulating the organic content of these sediments, it was possible to establish three treatments with similar BaP concentrations in the interstitial water, but differing in the amount of BaP in the bulk sediment. BaP bioaccumulation over the first few days of exposure was correlated with feeding rate, suggesting that ingested sediments were a source of BaP. The greatest body burden, however, was attained in those individuals held in sediments with the lowest organic carbon content and the lowest BaP concentration. Body burden at steady state was not correlated with either BaP concentrations in bulk sediment (dry weight or organic carbon-normalized bases) or the interstitial water. Increased organic matter decreased BaP bioavailability in a non-linear fashion. Bioaccumulation factors relative to water and organic content were relatively constant between 1 and 2% organic carbon in the sediment, but these same accumulation factors substantially underestimated body burden if applied to sandy sediments with little (0.3%) organic carbon.

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Literature cited

  • Adams, J. W. (1987). Bioavailability of neutral lipophilic organic chemicals contained in sediments: a review. In: Dickson, K. L., Maki, A. W., Brungs, W. A. (eds.) Fate and effects of sedimentbound chemicals in aquatic systems. Pergamon Press, New York, p. 219–244

    Google Scholar 

  • Adams, W. J., Kimerle, R. A., Mosher, R. G. (1985). Aquatic safety assessment of chemicals sorbed to sediments. In: Cardwell, R. D., Purdy, R., Bahner, R. C. (eds.) Aquatic toxicology and hazard assessment: Seventh Symposium. STP 854. American Society for Testing and Materials, Philadelphia, p. 429–453

    Google Scholar 

  • Anderson, J. W., Kiesser, S. L., Blaylock, J. W. (1979). Comparative uptake of naphthalenes from water and oiled sediment by benthic amphipods. In: Proceedings of the 1979 Oil Spill Conference. American Petroleum Institute, Washington, D.C., p. 579–584. (Publs Am. Petrol. Inst. No. 4308)

    Google Scholar 

  • Anderson, J. W., Moore, L. J., Blaylock, J. W., Woodruff, D. L., Kiesser, S. L. (1977). Bioavailability of sediment-sorbed naphthalenes to the sipunculid worm,Phascolosoma agassizii. In: Wolfe, D. A. (ed.) Fate and effects of petroleum hydrocarbons in marine organisms and ecosystems. Pergamon Press, New York, p. 276–285

    Google Scholar 

  • Augenfeld, J. M., Anderson, J. W., Riley, R. G., Thomas, B. L. (1982). The fate of polyaromatic hydrocarbons in an intertidal sediment exposure system: bioavailability toMacoma inquinata (Mollusca: Pelecypoda) andAbarenicola pacifica (Annelida: Polychaeta). Mar. envirl Res. 7: 31–50

    Google Scholar 

  • Baumfalk, Y. A. (1979). Heterogeneous grain size distribution in tidal flat sediment caused by bioturbation activity ofArenicola marina (Polychaeta). Neth. J. Sea. Res. 13: 428–440

    Google Scholar 

  • Beasley, T. M., Fowler, S. W. (1976). Plutonium and americium: uptake from contaminated sediments by the polychaeteNereis diversicolor. Mar. Biol. 38: 95–100

    Google Scholar 

  • Boehm, P. D., Quinn, J. G. (1976). The effect of dissolved organic matter in sea water on the uptake of mixed individual hydrocarbons and number 2 fuel oil by a marine bivalve (Mercenaria mercenaria). Estuar. cstl mar. Sci. 4: 93–105

    Google Scholar 

  • Boese, B. L., Lee, H., II, Sprecht, D. T., Randall, R. C., Winsor, M. (in press). Aqueous and solid phase HCB uptake in a depositfeeding clam. Envir. Toxic. Chem.

  • Bryan, G. W., Hummerstone, L. G. (1971). Adaptation of the polychaeteNereis diversicolor to estuarine sediments containing high concentrations of heavy metals. I. General observations and adaptations to copper. J. mar. biol. Ass. U. K. 51: 845–863

    Google Scholar 

  • Bryan, G. W., Uysal, H. (1978). Heavy metals in the burrowing bivalveScrobicularia plana from the Tamar Estuary in relation to environmental levels. J. mar. biol. Ass. U.K. 58: 89–108

    Google Scholar 

  • Cadée, G. C. (1976). Sediment reworking byArenicola marina on tidal flats in the Dutch Wadden Sea. Neth. J. Sea Res. 10: 440–460

    Google Scholar 

  • Chapman, P. M. (1989). Current approaches to developing sediment quality criteria. Envir. Toxic. Chem. 8: 589–599

    Google Scholar 

  • Collier, T. K. (1978). Disposition and metabolism of napthalene in rainbow trout (Salmo gairdneri). M.S. thesis. University of Washington, Seattle

    Google Scholar 

  • Eadie, B. J., Landrum, P. F., Faust, W. (1982). Polycyclic aromatic hydrocarbons in sediments, pore water and the amphipodPontoporeia hoyi from Lake Michigan. Chemosphere (U.K.) 11: 847–858

    Google Scholar 

  • Foster, G. D., Wright, D. A. (1988). Unsubstituted polynuclear aromatic hydrocarbons in sediments, clams, and clam worms from Chesapeake Bay. Mar. Pollut. Bull. 19: 459–465

    Google Scholar 

  • Fowler, S. W., Polikarpov, G. G., Elder, D. L., Parsi, P., Villeneuve, J.-P. (1978). Polychlorinated biphenyls: accumulation from contaminated sediments and water by the polychaeteNereis diversicolor. Mar. Biol. 48: 303–465

    Google Scholar 

  • Hedges, J. I., Stern, J. H. (1984). Carbon and nitrogen determinations of carbonate-containing solids. Limnol. Oceanogr. 29: 657–663

    Google Scholar 

  • Heitkamp, M. A., Cerniglia, C. E. (1987). Effects of chemical structure and exposure on the microbial degradation of polycyclic aromatic hydrocarbons in freshwater and estuarine ecosystems. Envir. Toxic. Chem. 6: 535–546

    Google Scholar 

  • Herbes, S. E., Schwall, L. R. (1978). Microbial transformation of polycylic aromatic hydrocarbons in pristine and petroleum-contaminated sediments. Appl. envirl Microbio. 35: 306–316

    Google Scholar 

  • Howell, R. (1983). Heavy metals in marine nematodes: uptake, tissue distribution and loss of copper and zinc. Mar. Pollut. Bull. 14: 263–268

    Google Scholar 

  • Hylleberg, J. (1975). Selective feeding byAbarenicola pacifica with notes onAbarenicola vagabunda and a concept of gardening in lugworms. Ophelia 14: 113–137

    Google Scholar 

  • Karickhoff, S. W. (1981). Semi-empirical estimation of sorption of hydrophobic pollutants on natural sediments and soils. Chemosphere 10: 833–846

    Google Scholar 

  • Kemp, P. F., Swartz, R. C. (1988). Acute toxicity of interstitial and particle-bound cadmium to a marine infaunal amphipod. Mar. envirl Res. 26: 135–153

    Google Scholar 

  • Klump, J. V., Krezoski, J. R., Smith, M. E., Kaster, J. L. (1987). Dual tracer studies of the assimilation of an organic contaminant from sediments by deposit feeding oligochaetes. Can. J. Fish. aquat. Sciences 44: 1574–1583

    Google Scholar 

  • Landrum, P. F., Nihart, S. R., Eadie, B. J., Herche, L. R. (1987). Reduction in bioavailability of organic contaminants to the amphipodPontoporeia hoyi by dissolved organic matter of sediment interstitial waters. Envir. Toxic. Chem. 6: 11–20

    Google Scholar 

  • Landrum, P. F., Reinhold, M. D. Nihart, S. R., Eadie, B. J. (1985). Predicting the bioavailability of organic xenobiotics toPontoporeia hoyi in the presence of humic and fulvic materials and natural dissolved organic matter. Envir. Toxic. Chem. 4: 459–467

    Google Scholar 

  • Langston, W. J. (1984). Availability of arsensic to estuarine and marine organisms: a field and laboratory evaluation. Mar. Biol. 80: 143–154

    Google Scholar 

  • Lee, R. F., Singer, S. C. (1980). Detoxifying enzymes system in marine polychaetes: increases in activity after exposure to aromatic hydrocarbons. Rapp. P.-v. Réun. Cons. perm. int. Explor. Mer 179: 29–32

    Google Scholar 

  • Leversee, G. J., Landrum, P. F., Giesy, J. P., Fannin, T. (1983). Humic acids reduce bioaccumulation of some polycyclic aromatic hydrocarbons. Can. J. Fish. aquat. Sciences 40 (Suppl. 2): 63–69

    Google Scholar 

  • Luoma, S. N., Bryan, G. W. (1982). A statistical study of environmental factors controlling concentrations of heavy metals in the burrowing bivalveScrobicularia plana and the polychaeteNereis diversicolor. Estuar., cstl Shelf Sci. 15: 95–108

    Google Scholar 

  • Luoma, S. N., Jenne, E. A. (1975). The availability of sedimentbound cobalt, silver and zinc to a deposit-feeding clam. In: Biological implications of metals in the environment. Energy Research and Development Administration, Springfield, Virginia, p. 213–230. (ERDA Symp. Ser. No. 42)

    Google Scholar 

  • Lyes, M. C. (1979). Bioavailability of a hydrocarbon from water and sediment to the marine wormArenicola marina. Mar. Biol. 55: 121–127

    Google Scholar 

  • Lynch, T. R., Johnson, H. E. (1982). Availability of a hexachlorobiphenyl isomer to benthic amphipods from experimentally contaminated natural sediments. In: Pearson, J. G., Foster, R. B., Bishop, W. E. (eds.) Aquatic toxicology and hazard assessment 766. American Society for Testing and Materials, Philadelphia, p. 273–287

    Google Scholar 

  • Mackay, D., Bobra, A., Shiu, W. Y. (1980). Relationships between aqueous solubility and octanol-water partition coefficients. Chemosphere (U.K.) 9: 701–711

    Google Scholar 

  • Malins, D. C., Krahn, M. M., Myers, M. S., Rhodes, L. D., Brown, D. W., Krone, C. A., McCain, B. B., Chan, S.-L. (1985). Toxic chemicals in sediments and biota from a creosote-polluted harbor: relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). Carcinogenesis 6: 1463–1469

    Google Scholar 

  • Matsumura, F. (1977). Absorption, accumulation and elimination of pesticides by aquatic organisms. In: Kahn, M. A. Q. (ed.) Pesticides in aquatic environments. Plenum Press, New York, p. 77–105

    Google Scholar 

  • McCarthy, J. F. (1983). Role of particulate organic matter in decreasing accumulation of polynuclear aromatic hydrocarbons byDaphnia magna. Archs envir. Contam. Toxic. 12: 559–568

    Google Scholar 

  • McElroy, A. E. (1985).In vivo metabolism of benz (a) anthracene by the polychaeteNereis virens. Mar. envirl Res. 17: 133–136

    Google Scholar 

  • McElroy, A. E., Farrington, J. W., Teal, J. M. (1989). Bioavailability of polycyclic aromatic hydrocarbons in the aquatic environment. In: Varanasi, U. (ed.) Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment. CRC Press, Boca Raton, Florida, p. 1–39

    Google Scholar 

  • McLeese, D. W., Metcalfe, C. D., Pezzack, D. S. (1980). Uptake of PCBs from sediment byNereis virens andCrangon septemspinosa. Archs envir. Contam. Toxic. 9: 507–518.

    Google Scholar 

  • Miller, M. M., Wasik, S. P., Huang, G.-L., Wan-Ying Shiu, S., Mackay, D. (1985). Relationships between octanol-water partition coefficient and aqueous solubility. Envir. Sci. Technol. 19: 522–529

    Google Scholar 

  • Miramand, P., Germain, P., Camus, H. (1982). Uptake of americium and plutonium from contaminated sediments by three benthic species:Arenicola marina, Corophium volulator andScrobicularia plana. Mar. Ecol. Prog. Ser. 7: 59–65

    Google Scholar 

  • Muir, D. C. G., Townsend, B. E., Lockhart, W. L. (1983). Bioavailability of six organic chemicals toChironomus tentans larvae in sediment and water. Envir. Toxic. Chem. 2: 269–281

    Google Scholar 

  • Murphy, P. G., Murphy, J. V. (1971). Correlations between respiration and direct uptake of DDT in the mosquito fish,Gambusia affinis. Bull. envir. Contam. Toxic. 6: 581–588

    Google Scholar 

  • Pavlou, S. P. (1984). The use of the equilibrium partitioning approach in determining safe levels of contaminants in marine sediments. In: Dickson, K. L., Maki, A. W., Brungs, W. A. (eds.) Fate and effects of sediment-bound chemicals in aquatic systems. Pergamon Press, New York, p. 388–412

    Google Scholar 

  • Payne, J. F. (1977). Mixed function oxidases in marine organisms in relation to petroleum hydrocarbon metabolism and detection. Mar. Pollut. Bull. 8: 112–116

    Google Scholar 

  • Penry, D. L., Jumars, P. A. (1987). Modeling animal guts as chemical reactors. Am. Nat. 129: 69–96

    Google Scholar 

  • Pesch, C. E., Morgan D. (1978). Influence of sediment in copper toxicity tests with the polychaeteNeanthes arenaceodentata. Wat. Res. 12: 747–751

    Google Scholar 

  • Radding, S. B., Mill, T., Gould, C. W., Liu, D. H., Johnson, H. L., Bomberger, D. C., Fojo, C. V. (1976). The environmental fate of selected polynuclear aromatic hydrocarbons. U.S. Environmental Protection Agency, Washington, D. C. (EPA 560/5-75-009)

    Google Scholar 

  • Rapaport, R. A., Eisenrich, S. J. (1984). Chromatographic determination of octanol-water partition coefficients for 58 polychlorinated biphenyl congeners. Envir. Sci. Technol. 18: 163–170

    Google Scholar 

  • Reichert, W. L., Le Eberhard, B.-T., Varanasi, U. (1985). Exposure of two species of deposit-feeding amphipods to sediment-associated [3H]benzo [a] pyrene: uptake, metabolism and covalent binding to tissue macromolecules. Aquat. Toxic 6: 45–56.

    Google Scholar 

  • Roesijadi, G., Anderson, J. W., Blaylock, J. W. (1978a). Uptake of hydrocarbons from marine sediments contaminated with Prudhoe Bay crude oil: influence of feeding type of test species and availability of polycyclic aromatic hydrocarbons. J. Fish. Res. Bd Can. 35: 608–614

    Google Scholar 

  • Roesijadi, G., Woodruff, D. L., Anderson, J. W. (1978b). Bioavailability of naphthalenes from marine sediments artificially contaminated with Prudhoe Bay crude oil. Envir. Pollut. 15: 223–229

    Google Scholar 

  • Rossi, S. S. (1977). Bioavailability of petroleum hydrocarbons from water, sediments, and detritus to the the marine annelid,Neanthes arenaceodentata. In: Proceedings of the 1977 Oil Spill Conference. American Petroleum Institute, Washington, D.C. p. 621–625. (Publs Am. Petrol. Inst. No. 4284)

    Google Scholar 

  • Self, R. F. L., Jumars, P. A. (1988). Cross-phyletic patterns of particle selection by deposit feeders. J. mar. Res. 46: 119–143

    Google Scholar 

  • Servos, M. R., Muir, D. C. G. (1989). Effect of dissolved organic matter from Canadian Shield lakes on the bioavailability of 1, 3, 6, 8-tetrachlorodibenzo-p-dioxin to the amphipodCrangonyx laurentianus. Envir. Toxic. Chem. 8: 141–150

    Google Scholar 

  • Socha, S. B., Carpenter, R. (1987). Factors affecting pore water hydrocarbon concentrations in Puget Sound sediments. Geochim. cosmochim. Acta 51: 1273–1284

    Google Scholar 

  • Stein, J. E., Hom, T., Casillas, E., Friedman, A., Varanasi, U. (1987). Simultaneous exposure of English sole (Parophrys vetulus) to sediment-associated xenobiotics: Part 2—Chronic exposure to an urban estuarine sediment with added3H-benzo[a]pyrene and14C-polychlorinated biphenyls. Mar. envirl Res. 22: 123–149

    Google Scholar 

  • Taghon, G. L., Greene, R. R. (in press). Effects of sediment protein concentration on feeding and growth rates ofAbarenicola pacifica Healy and Wells (Polychaeta: Abarencolidae). J. exp. mar. Biol. Ecol.

  • Taghon, G. L., Jumars, P. A. (1984). Variable ingestion rate and its role in optimal foraging behavior of marine deposit feeders. Ecology 65: 549–558

    Google Scholar 

  • Ueda, T., Nakamua, R., Suzuki, Y. (1976). Comparison of115mCd accumulation from sediments and sea water by polychaete worms. Bull. Jap. Soc. scient. Fish. 42: 299–306

    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 

  • Yang, S. K., Gelboin, H. V., Trump, B. N., Autrup, H. N., Harris, C. C. (1977). Metabolic activitation of benzo(a)pyrene and binding to DNA in cultured human bronchus. Cancer Res. 37: 1210–1215

    Google Scholar 

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Communicated by M. G. Hadfield, Honolulu

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Weston, D.P. Hydrocarbon bioaccumulation from contaminated sediment by the deposit-feeding polychaeteAbarenicola pacifica . Mar. Biol. 107, 159–169 (1990). https://doi.org/10.1007/BF01313253

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