Skip to main content

Advertisement

Log in

Time-course uptake and elimination of benzo(a)pyrene and its damage to reproduction and ensuing reproductive outputs of Pacific oyster, Crassostrea gigas

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The time-course of uptake and elimination of benzo(a)pyrene (BaP) for the Pacific oyster, Crassostrea gigas and reproduction damage and reproductive outputs were studied. Sexually immature C. gigas broodstock were fed for 28 days with live algae grown in four BaP solutions of 0, 50, 500, and 5,000 μg L−1 (hereafter, control, 50, 500, and 5,000 oysters) and were subsequently conditioned to maturation by a feeding with BaP-free live algae under temperature manipulation for another 28 days. The 5,000 μg L−1 oysters gained a steady state concentration, around 30,000 ng g−1 d.w. for digestive gland, a week earlier compared to the 500 μg L−1 oysters. The earlier gain or longer persistence of the steady state concentration influenced elimination of BaP, with an eliminating trend for 500 μg L−1 oysters, while no elimination for 5,000 μg L−1 oysters. The maternal persistence of the steady state concentration resulted in significant damages in the reproductive success and their reproductive outputs in terms of the hatching rate and larval growth, survival, and settlement. The 50 μg L−1 oysters remained far below the steady state concentration, and showed a manifest eliminating behavior during the subsequent BaP-free 28 day maturation period. The reproductive success and initial larval events of 50 μg L−1 oysters were comparable to those of control. However, the damage potential of the 50 μg L−1 oysters might be more significant if their maternal exposure continued beyond 28 days, since the accumulation profile at this dose was linear.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aarab N, Minier C, Lemaire S, Unruh E, Hansen P-D, Larsen BK, Andersen O-K, Narbonne J-F (2004) Biochemical and histological responses in mussel (Mytilus edulis) exposed to North Sea oil and a mixture of North Sea oil and alkylphenols. Mar Environ Res 58:437–441

    Article  CAS  Google Scholar 

  • Achard M, Baudrimont M, Boudou A, Bourdineaud JP (2004) Induction of a multixenobiotic resistance protein (MXR) in the Asiatic clam Corbicula fluminea after heavy metals exposure. Aquat Toxicol 67:347–357

    Article  CAS  Google Scholar 

  • Akcha F, Burgeot T, Venier P, Budzinski H, Narbonne JF (1999) Relationship between kinetics of benzo(a)pyrene bioaccumulation and DNA binding in the mussel Mytilus galloprovincialis. Bull Environ Contam Toxicol 62:455–462

    Article  CAS  Google Scholar 

  • Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbonne JF (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo(a)pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat Toxicol 49:269–287

    Article  CAS  Google Scholar 

  • Auffret M, Oubella R. (1997) Hemocyte aggregation in the oyster Crassostrea gigas: in vitro measurement and experimental modulation by xenobiotics. Comp Biochem Physiol 118A:705–712

    Article  CAS  Google Scholar 

  • Bard SM (2000) Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aquat Toxicol 48:357–389

    Article  CAS  Google Scholar 

  • Bigger CAH, Cheh A, Latif F, Fishel R, Canella KA, Stafford GA, Yagi H, Jerina DM, Dipple A (1994) DNA strand breaks induced by configurationally isometric hydrocarbon diol epoxides. Drug Metab Rev 26:287–299

    Article  CAS  Google Scholar 

  • Baumard P, Budzinski H, Garrigues P, Narbonne JF, Burgeot T, Miche X, Bellocq J (1999) Polycyclic aromatic hydrocarbon (PAH) burden of mussels (Mytilus sp.) in different marine environments in relation with sediment PAH contamination, and bioavailability. Mar Environ Res 47:415–439

    Article  CAS  Google Scholar 

  • Cavalieri EL, Rogan EG, Murray WJ, Ramakrishna NVS (1993a) Mechanistic aspects of benzo(a)pyrene metabolism. Poly Aromat Comp 3:1047–1154

    CAS  Google Scholar 

  • Cavalieri EL, Rogan EG, Ramakrishna NVS, Devanesan PD (1993b) Mechanisms of benzo(a)pyrene and 7,12-dimethylbenzo(a)-anthrancene activation: qualitative aspects of the stable and depurination DNA adducts obtained from radical cations and diol epoxides. Poly Aromat Comp 3:725–731

    CAS  Google Scholar 

  • Cheung CCC, Zheng GJ, Li AMY, Richardson BJ, Lam PKS (2001) Relationship between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquat Toxicol 52:189–203

    Article  CAS  Google Scholar 

  • Choi W-J, Chun Y-Y, Park J-H, Park Y-C (1997) The influence of environmental characteristics on the fatness of Pacific oyster, Crassostrea gigas, in Hansan-Koje Bay. J Kor Fish Sci Technol 30:94–803

    Google Scholar 

  • Choy EJ, Jo Q, Do JW, Kim SS, Jee YJ, Min KS (2003) Properties of two biomarker parameters in the blood of farmed Pacific oyster, Crassostrea gigas, exposed to polychlorinated biphenyls. J Fish Sci Technol 6:74–80

    CAS  Google Scholar 

  • Chu F-LE, Soudant P, Cruz-Rodriguez LA, Hale RC (2000) PCB uptake and accumulation by feeding oysters Crassostrea virginica with PCB-sorbed algal paste. Mar Environ Res 50:217–221

    Article  CAS  Google Scholar 

  • Chu F-LE, Soudant P, Hale RC (2003) Relationship between PCB accumulation and reproductive output in conditioned oysters Crassostrea virginica fed a contaminated algal diet. Aquat Toxicol 65:293–307

    Article  CAS  Google Scholar 

  • Connell DW, Chaisuksant Y, Yu J (1999) Importance of internal biotic concentrations in risk evaluations with aquatic systems. Mar Pollut Bull 39:54–61

    Article  CAS  Google Scholar 

  • Eertman RHM, Groenink CLFMG, Sandee B, Hummel H (1995) Response of the blue mussel Mytilus edulis L. following exposure to PAHs or contaminated sediment. Mar Environ Res 39:169–173

    Article  CAS  Google Scholar 

  • Gagnaire B, Thomas-Guyon H, Burgeot Th, Renault T (2005) Pollutant effects on Pacific oyster, Crassostrea gigas (Thunberg), hemocytes: screening of 23 molecules using flow cytometry. Cell Biol Toxicol 22:1–14

    Article  Google Scholar 

  • Geffard O, Budzinski H, His E (2002a) The effects of elutriates from PAH and heavy metal polluted sediments on Crassostrea gigas (Thunberg) embryogenesis, larval growth and bio-accumulation by the larvae of pollutants from sedimentary origin. Ecotoxicol 11:403–416

    Article  CAS  Google Scholar 

  • Geffard O, Budzinski H, His E, Seaman MNL, Garrigues P (2002b) Relationships between contaminant levels in the marine sediments and their biological effects upon embryos of oysters, Crassostrea gigas. Environ Toxicol Chem 21:2310–2318

    Article  CAS  Google Scholar 

  • Geffard O, His E, Budzinski H, Chiffoleau JF, Coynel A, Etcheber H (2004) Effects of storage method and duration on the toxicity of marine sediments to embryos of Crassostrea gigas. Environ Pollut 129:457–465

    Article  CAS  Google Scholar 

  • Guerra-Rivas G, Gomez-Gutierrez CM, Marquez-Rocha FJ (2002) Effect of polycyclic aromatic hydrocarbons on the pallial fluid buffering capacity of the marine mussel, Mytilus galloprovinvialis. Comp Biochem Physiol 132C:171–179

    CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana and Detonula confervaceae Hustedt (Cleve). Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  • Hellou J, Law RJ (2003) Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health. Environ Pollut 126:407–416

    Article  CAS  Google Scholar 

  • His E, Seaman MNL, Beiras R (1997) A simplification of the bivalve embryogenesis larval development bioassay method for water quality assessment. Water Res 31:351–355

    Article  CAS  Google Scholar 

  • Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 196:191–205

    Article  CAS  Google Scholar 

  • Jo Q, Choy EJ, Park DW, Jee YJ, Kim SY, Kim Y (2002) Cellular biomarker of membrane stability and hydrolytic enzyme activity in the hemocytes of benzo(a)pyrene-exposed Pacific oyster, Crassostrea gigas. J Fish Sci Tech 5:263–270

    CAS  Google Scholar 

  • Jo Q, Moon HB, Cho YC, Kim KS, Choy EJ, Ko SC, Song YC (2005) Effects of sediment elutriates on the early reproductive outputs in the Pacific oyster, Crassostrea gigas. J Fish Sci Tech 8:27–33

    Google Scholar 

  • Kang C-K, Park MS, Lee P-Y, Choi W-J, Lee W-C (2000) Seasonal variations in condition, reproductive activity, and biochemical composition of the Pacific oyster, Crassostrea gigas (Thunberg), in suspended culture in two coastal bays of Korea. J Shell Res 19:771–778

    Google Scholar 

  • Kirso U, Irha N (1998) Role of algae in fate of carcinogenic polycyclic aromatic hydrocarbons in the aquatic environment. Ecotoxicol Environ Saf 41:83–89

    Article  CAS  Google Scholar 

  • Krasnoschekova R, Kirso U, Perin F, Jacquignon P (1992) Binding of heteropolyarenes to protein. Poly Aromat Comp 3:41–49

    Article  CAS  Google Scholar 

  • Kurelec B, Pivcevic B (1991) Evidence for a multixenobiotic resistance mechanism in the mussel Mytilus galloprovincialis. Aquat Toxicol 19:291–302

    Article  CAS  Google Scholar 

  • Kurelec B (1992) The multixenobiotic resistance mechanism in aquatic organisms. Crit Rev Toxicol 22:23–43

    Article  CAS  Google Scholar 

  • Law RJ, Kelly CA, Baker KL, Langford KH, Bartlett T (2002) Polycyclic aromatic hydrocarbons in sediments, mussels and crustacea around a former gasworks site in Shoreham-by-Sea, UK. Mar Pollut Bull 44:903–911

    Article  CAS  Google Scholar 

  • Li S-C, Wang W-X, Hsieh D (2001) Feeding and absorption of the toxic dinoflagellate Alexandrium tamarense by two marine bivalves from the South China Sea. Mar Biol 139:617–624

    Article  Google Scholar 

  • Li Q, Osada M, Takahashi K, Matsutani T, Mori K (1997) Accumulation and depuration of tributyltin oxide and development in the Pacific oyster, Crassostrea gigas. Bull Environ Contam 58:489–496

    Article  CAS  Google Scholar 

  • Livingstone DR, Arnold R, Chipman JK, Kirchin MA, Marsh J (1990) The mixed-function oxygenase system in molluscs: metabolism, responses to xenobiotics, and toxicity. Oceanis 16:331–347

    CAS  Google Scholar 

  • Livingstone DR, Chipman JK, Lowe MD, Minier C, Mitchelmore CL, Moore MN, Peters LD, Pipe RK (2000) Development of biomarkers to detect the effects of organic pollution on aquatic invertebrates: recent molecular, genotoxic, cellular and immunological studies on the common mussel (Mytilus edulis L.) and other mytilids. Intl J Environ Pollut 13:56–91

    Article  CAS  Google Scholar 

  • Lyons BP, Pascoe CK, McFadzen IRB (2002) Phototoxicity of pyrene and benzo(a)pyrene to embryo-larval stages of the pacific oyster Crassostrea gigas. Mar Environ Res 54:627–631

    Article  CAS  Google Scholar 

  • Maccubbin AE (1994) DNA adduct analysis in fish: laboratory and field studies. In: Malins DC, Ostrander GK (eds) Aquatic toxicology: molecular, biochemical and cellular perspectives. CRC Press, Boca Raton, pp 267–294

    Google Scholar 

  • Mitchelmore CL, Claudia BJ, Chipman K, Livingstone DR (1998) Evidence for cytochrome P−450 catalysis and free radical involvement in the production of DNA strand breaks by benzo(a)pyrene and nitroaromatics in mussel (Mytilus edulis L.) digestive gland cells. Aquat Toxicol 41:193–212

    Article  CAS  Google Scholar 

  • Moon HB (2003) Fate of dioxins and dioxin-like contaminants in the coastal environment of Korea. Ph. D. Thesis. Department of Environmental Atmospheric Sciences, Pukyong National University, Busan pp 1–307

  • Moy FE, Walday M (1996) Accumulation and depuration of organic micro-pollutants in marine hard bottom organisms. Mar Pollut Bull 33:56–63

    Article  CAS  Google Scholar 

  • Næs K, Oug E, Knutzen J (1998) Source and species-dependent accumulation of polycyclic aromatic hydrocarbons (PAHs) in littoral indicator organisms from norwegian smelter-affected marine waters. Mar Environ Res 45:193–207

    Article  Google Scholar 

  • Narbonne JF, Djomo JE, Ribera D, Ferrier V, Garrigues P (1999) Accumulation kinetics of polycyclic aromatic hydrocarbons absorbed to sediment by the mollusk Corbicular fluminea. Ecotoxicol Environ Saf 42:1–8

    Article  CAS  Google Scholar 

  • Noreña-Barroso E, Gold-Bouchot G, Zapata-Perez O, Sericano JL (1999) Polynuclear Aromatic Hydrocarbons in American Oysters Crassostrea virginica from the Terminos Lagoon, Campeche, Mexico. Mar Poll Bull 38: 637–645

    Article  Google Scholar 

  • Okay OS, Donkin P, Peters LD, Livingstone DR (2000) The role of algae (Isochrysis galbana) enrichment on the bioaccumulation of benzo(a)pyrene and its effects on the blue mussel Mytilus edulis. Environ Pollut 110:103–113

    Article  CAS  Google Scholar 

  • Page DS, Boehm PD, Brown JS, Neff JM, Burns WA, Bence AE (2005) Mussels document loss of bioavailable polycyclic aromatic hydrocarbons and the return to baseline conditions for oiled shorelines in Prince William Sound, Alaska. Mar Environ Res 60:422–436

    Article  CAS  Google Scholar 

  • Park DW, Jo Q, Lim HJ, Veron B (2002) Sterol composition of dark-grown Isochrysis galbana and its implication in the seed production of Pacific oyster, Crassostrea gigas. J Appl Phycol 14:351–355

    Article  Google Scholar 

  • Park MS, Lim HJ, Kim PJ (1998) Effect of environmental factors on the growth, glycogen and hemoglobin content of cultured arkshell, Scapharca broughtonii. J Kor Fish Sci Tech 31:176–185

    CAS  Google Scholar 

  • Park MS, Lim HJ, Jo Q, Yoo JS, Jeon M (1999) Assessment of reproductive health in the wild seed oysters, Crassostrea gigas, from two locations in Korea. J Shell Res 18:445–450

    Google Scholar 

  • Peachey RL, Crosby DG (1996) Phototoxicity in tropical reef animals. Mar Environ Res 42:359–362

    Article  CAS  Google Scholar 

  • Pelletier MC, Burgess RM, Cantwell MG, Serbst JR, Ho KT, Ryba SA (2000) Importance of maternal transfer of the photoreactive polycyclic aromatic hydrocarbon fluoranthene from benthic adult bivalves to their pelagic larvae. Environ Toxicol Chem 19:2691–2698

    Article  CAS  Google Scholar 

  • Pérez-Cadahía B, Laffon B, Pásaro E., Méndez J (2004) Evaluation of PAH bioaccumulation and DNA damage in mussels (Mytilus galloprovincialis) exposed to spilled Prestige crude oil. Comp Biochem Physiol 38C:453–460

    Google Scholar 

  • Qian Y, Wade TL, Sericano JL (2001) Sources and bioavailability of polynuclear aromatic hydrocarbons in Galveston Bay, Texas. Estuaries 24: 817–827

    Article  CAS  Google Scholar 

  • Rasmussen JB, Rowan DJ, Lean DRS, Carey JH (1990) Food chain structure in Ontario lakes determines PCB levels in lake trout (Salvelinus namaycush) and other pelagic fish. J Can Fish Aquat Sci 47:2030–2038

    Article  Google Scholar 

  • SPSS (2000) SPSS base 10.0 user’s guide. Chicago, IL: SPSS Inc

  • Stegeman JJ (1985) Benzo(a)pyrene oxidation and microsomal enzyme activity in the mussel (Mytilus edulis) and other bivalve mollusc species from the Western North Atlantic. Mar Biol 89:21–30

    Article  CAS  Google Scholar 

  • Smital T, Kurelec B (1997) Inhibition of the mutixenobiotic resisitance mechanism in natural waters: in vivo demonstration of their effects. Environ Toxicol Chem 16:2164–2170

    Article  CAS  Google Scholar 

  • Tilghman Hall A, Oris JT (1991) Anthracene reduces reproductive potential is maternally transferred during long-term exposure in fathead minnows. Aquat Toxicol 19: 249–264

    Article  Google Scholar 

  • Van der Oost R, Heida H, Opperhuizen A (1998) Polychlorinated biphenyl congeners in sediments, plankton, molluscs, crustaceans, and eel in a freshwater lake: implications of using reference chemicals and indicator organisms in bioaccumulation studies. Arch Environ Contam Toxicol 17:721–729

    Article  Google Scholar 

  • Venier P, Canova S (1996) Formation of DNA adducts in the gill tissue of Mytilus galloprovincialis treated with benzo(a)pyrene. Aquat Toxicol 34:119–133

    Article  CAS  Google Scholar 

  • White P (2002) The genotoxicity of priority polycyclic aromatic hydrocarbons in the complex mixtures. Mutat Res 515:85–98

    Article  CAS  Google Scholar 

  • Wohlgeschaffen GD, Mann KH, Rao DVS, Pocklington R (1996) Dynamics of the phycotoxin domoic acid: accumulation and excretion in two commercially important bivalves. J Appl Phycol 4:297–310

    Article  Google Scholar 

Download references

Acknowledgments

The research was funded by National Fisheries Research and Development Institute, Ministry of Maritime Affairs and Fisheries, South Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qtae Jo.

Additional information

Communicated by S. Nishida, Tokyo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Choy, E.J., Jo, Q., Moon, HB. et al. Time-course uptake and elimination of benzo(a)pyrene and its damage to reproduction and ensuing reproductive outputs of Pacific oyster, Crassostrea gigas . Mar Biol 151, 157–165 (2007). https://doi.org/10.1007/s00227-006-0464-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0464-4

Keywords

Navigation