Skip to main content
Log in

Effect of the Hebei Spirit Oil Spill on the Condition, Reproduction, and Energy Storage Cycle of the Manila Clam Ruditapes philippinarum on the West Coast of Korea

  • Special Issue: Climate Change and Anthropogenic Change around Korean Peninsula
  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Seasonal variations in the condition, biochemical composition, and reproduction of Ruditapes philippinarum were investigated from August 2009 to October 2010, 18 months after the Hebei Spirit oil spill off Malipo Beach on the west coast of Korea. No significant differences in physical and nutritional conditions were found between the oil-damaged and the undamaged control beaches. At the undamaged Mongsanpo Beach, all the biometric components (dry tissue weights and biochemical components) remained at low levels during autumn–winter but increased rapidly through spring, followed by a dramatic drop in August. In contrast, at the oil-damaged beach, no clear seasonal fluctuations were detected in the biometric components during the study period. Absolute values of all the components were much higher at the control than at the damaged site. This lack of energy reserves in the clams in the damaged area likely resulted in a failure of gametogenic development. Gonadal maturity index peaked in summer at both beaches. However, the gross egg weight was much higher at the control than at the damaged site during June–July. In addition, its different peak timing between sites indicated a month’s lag in the major spawning pulse at the oil-damaged beach. The spatial variations in all the biometric components of the clams observed in this study clearly implied that the Hebei Spirit oil spill may interfere with the clam phenology at Malipo Beach within 2 to 3 years after the incident.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adachi, K. 1979. Seasonal changes of the protein level in the adductor muscle of the clam, Tapes philippinarum (Adams and Reeve) with special reference to the reproductive seasons. Comparative Biochemistry and Physiology 64: 85–89.

    Article  Google Scholar 

  • Ansell, A.D., and A. Trevallion. 1967. Studies on Tellina tenuis de Costa: I. Seasonal growth and biochemical cycle. Journal of Experimental Marine Biology and Ecology 1 (2): 220–235.

    Article  Google Scholar 

  • Bayne, B.L. 1976. Aspects of reproduction in bivalve mollusks. In Estuarine processes, ed. M.L. Wiley, 432–448. New York: Academic Press.

    Chapter  Google Scholar 

  • Bayne, B.L., and C.M. Worrall. 1980. Growth and production of mussels Mytilus edulis from two populations. Marine Ecology Progress Series 3: 317–318.

    Article  Google Scholar 

  • Bayne, B.L., D.L. Holland, M.N. Moore, D.M. Lowe, and J. Widdows. 1978. Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. Journal of the Marine Biological Association of United Kingdom 51: 659–668.

    Google Scholar 

  • Bayne, B.L., J. Widdows, M.N. Moore, P. Salkeld, C.M. Worrall, and P. Donkin. 1982. Some ecological consequences of the physiological and biochemical effects of petroleum compounds on marine molluscs. Philosophical Transactions of the Royal Society of London B 297 (1087): 219–239.

    CAS  Google Scholar 

  • Beninger, P.G., and A. Lucas. 1984. Seasonal variations in condition, reproductive activity, and gross biochemical composition of two species of adult clam reared in a common habitat: Tapes decussates (L.) (Jeffreys) and Tapes philippinarum (Adams and Reeve). Journal of Experimental Marine Biology and Ecology 79 (1): 19–37.

    Article  CAS  Google Scholar 

  • Bligh, E.G., and W.J. Dyer. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37 (1): 911–917.

    Article  CAS  Google Scholar 

  • Capuzzo, J.M., and D.F. Leavitt. 1988. Lipid composition of the digestive glands of Mytilus edulis and Carcinus maenas in response to pollution gradients. Marine Ecology Progress Series 46: 139–145.

    Article  CAS  Google Scholar 

  • Chu, F.E., P. Soudant, and R.C. Hale. 2003. Relationship between PCB accumulation and reproductive output in conditioned oysters Crassostrea virginica fed a contaminated algal diet. Aquatic Toxicology 65 (3): 293–307.

    Article  CAS  Google Scholar 

  • Culbertson, J.B., I. Valiela, Y.S. Olsen, and C.M. Reddy. 2008. Effect of field exposure to 38-year-old residual petroleum hydrocarbons on growth, condition index, and filtration rate of the robbed mussel, Geukensia demissa. Environmental Pollution 154 (2): 312–319.

    Article  CAS  Google Scholar 

  • Dame, R.F. 1996. Bivalves as components of ecosystem health. In The ecology of marine bivalves. An ecosystem approach, ed. R.F. Dame, 213–226. Boca Raton, FL: CRC Press.

    Chapter  Google Scholar 

  • Dare, P.J., and G. Davies. 1975. Experimental suspended culture of mussels, Mytilus edulis (L), in Wales using spat transplanted from a distant settlement ground. Aquaculture 6 (3): 257–274.

    Article  Google Scholar 

  • Dinamani, P. 1987. Gametogenic patterns in populations of Pacific oyster, Crassostrea gigas, in Northland, New Zealand. Aquaculture 64 (1): 65–76.

    Article  Google Scholar 

  • Donaghy, L., H.K. Hong, M. Kim, H.S. Park, and K.W. Choi. 2016. Assessment of the fitness of the mussel Mytilus galloprovincialis two years after the Hebei Spirit oil spill. Marine Pollution Bulletin 113 (1-2): 324–331.

    Article  CAS  Google Scholar 

  • Dubois, M., K.A. Gilles, J.K. Hamilton, P.A. Rebecs, and F. Smith. 1956. Colorimetric method for the determination of sugars and related substances. Analytical Chemistry 28 (3): 350–356.

    Article  CAS  Google Scholar 

  • Duquesne, S., M. Liess, and D.J. Bird. 2004. Sublethal effects of metal exposure: Physiological and behavioural responses of the estuarine bivalve (Macoma balthica). Marine Environmental Research 58 (2-5): 245–250.

    Article  CAS  Google Scholar 

  • Frouin, H., J. Pellerin, M. Fournier, E. Pelletier, P. Richard, N. Pichaud, C. Rouleau, and F. Garnerot. 2007. Physiological effects of polycyclic aromatic hydrocarbons on soft-shell clam Mya arenaria. Aquatic Toxicology 82 (2): 120–134.

    Article  CAS  Google Scholar 

  • Gabbott, P.A. 1983. Development and seasonal metabolic activities in marine mollusks. In The Mollusca, ed. A.S.M. Saleuddin and K.M. Wilbur, 165–217. New York: Academic Press.

    Chapter  Google Scholar 

  • Gilfillan, E.S., and J.H. Vandermeulen. 1978. Alterations in growth and physiology in chronically oiled soft-shell clams, Mya arenaria, chronically oiled with bunker C form Chedabucto Bay, Nova Scotia 1970–76. Journal of the Fisheries Research Board of Canada 35 (5): 630–636.

    Article  CAS  Google Scholar 

  • Holland, D.L. 1978. Lipid reserves and energy metabolism in the larvae of benthic marine invertebrates. In Biochemical and biophysical perspectives in marine biology, ed. D.C. Malins and J.R. Sargent, 85–123. London: Academic Press.

    Google Scholar 

  • Hong, H.K., L. Donaghy, C.K. Kang, H.S. Kang, H.J. Lee, H.S. Park, and K.W. Choi. 2016. Substantial changes in hemocyte parameters of Manila clam Ruditapes philippinarum two years after the Hebei Spirit oil spill off the west coast of Korea. Marine Pollution Bulletin 108 (1-2): 171–179.

    Article  CAS  Google Scholar 

  • Humanson, G.L. 1979. Animal Tissue Technique. San Francisco: Freeman and Company.

    Google Scholar 

  • Hummel, H., R.H. Bogaards, J. Nieuwenhuise, L. de Wolf, and J.M. van Liere. 1990. Spatial and seasonal differences in PCB content of the mussel Mytilus edulis. Science of the Total Environment 92: 155–163.

    Article  CAS  Google Scholar 

  • Jackson, J.B.C., J.D. Cubit, B.D. Keller, V. Batista, K. Burns, H.M. Caffey, R.L. Caldwell, S.D. Garrity, C.D. Getter, C. Conzalez, H.M. Guzman, K.W. Kaufmann, A.H. Knap, S.C. Levings, M.J. Marshall, R. Steger, R.C. Thompson, and E. Weil. 1989. Ecological effects of a major oil spill on Panamanian coastal marine communities. Science 243 (4887): 37–44.

    Article  CAS  Google Scholar 

  • Jensen, K.T. 1993. Density-dependent growth in cockles (Cerastoderma edule): Evidence from interannual comparisons. Journal of Marine Biological Association of United Kingdom 73 (02): 333–342.

    Article  Google Scholar 

  • Ji, K., J. Seo, X. Liu, J. Lee, S. Lee, W. Lee, J. Park, J.S. Khim, S. Hong, Y. Choi, W.J. Shim, S. Takeda, J.P. Giesy, and K. Choi. 2011. Genotoxicity and endocrine-disruption potentials of sediment near an oil spill site: Two years after the Hebei Spirit oil spill. Environmental Science and Technology 45 (17): 7481–7488.

    Article  CAS  Google Scholar 

  • Kang, C.K., M.S. Park, P.Y. Lee, W.J. Choi, and W.C. Lee. 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. Journal of Shellfish Research 19: 771–778.

    Google Scholar 

  • Kang, S.G., K.S. Choi, A.A. Bulgakov, Y. Kim, and S.Y. Kim. 2003. Enzyme-linked immunosorbent assay (ELISA) used in quantification of reproductive output in the Pacific oyster, Crassostrea gigas, in Korea. Journal of Experimental Marine Biology and Ecology 282 (1-2): 1–21.

    Article  Google Scholar 

  • Kang, C.K., Y.S. Kang, E.J. Choy, D.S. Kim, B.T. Shim, and P.Y. Lee. 2007. Condition, reproductive activity, and gross biochemical composition of the Manila clam, Tapes philippinarum in natural and newly created sandy habitats of the southern coast of Korea. Journal of Shellfish Research 26 (2): 401–412.

    Article  Google Scholar 

  • Keck, R.T., R.C. Heess, J. Wehmiller, and D. Maurer. 1978. Sub-lethal effects of the water soluble fraction of Nigerian crude oil on the juvenile hard clams, Mercenaria mercenaria (Linne). Environmental Pollution 15 (2): 109–119.

    Article  CAS  Google Scholar 

  • Kim, M., U.H. Yim, S.H. Hong, J.H. Jung, H.W. Choi, J. An, J. Won, and W.J. Shim. 2010. Hebei Spirit oil spill monitored on site by fluorometric detection of residual oil in coastal water off Taean, Korea. Marine Pollution Bulletin 60 (3): 383–389.

    Article  CAS  Google Scholar 

  • Labarta, U., M.J. Fernández-Reiriz, J.L. Garrido, J.M.F. Babarro, J.M. Bayona, and J. Albaiges. 2005. Response of mussel recruits to pollution from the ‘Prestige’ oil spill along the Galicia coast. A biochemical approach. Marine Ecology Progress Series 302: 135–145.

    Article  CAS  Google Scholar 

  • Laffon, B., T. Rábade, E. Pásaro, and J. Méndez. 2006. Monitoring of the impact of Prestige oil spill on Mytilus galloprovincialis from Galician coast. Environment International 32 (3): 342–348.

    Article  CAS  Google Scholar 

  • Livingstone, D.R. 1993. Biotechnology and pollution monitoring: Use of molecular biomarkers in the aquatic environment. Journal of Chemical Technology and Biotechnology 57: 195–211.

    Article  CAS  Google Scholar 

  • Lowe, D.M., and R.K. Pipe. 1986. Hydrocarbon exposure in mussels: A quantitative study of the responses in the reproductive and nutrient storage cell systems. Aquatic Toxicology 8 (4): 265–272.

    Article  CAS  Google Scholar 

  • Lowry, O.M., N.I. Roseborough, A.L. Farrand, and R.J. Randall. 1951. Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193: 263–275.

    Google Scholar 

  • Lucas, A., and P.G. Beninger. 1985. The use of physiological condition indices in marine bivalve aquaculture. Aquaculture 44 (3): 187–200.

    Article  Google Scholar 

  • Mann, R. 1979. The effects of temperature on growth, physiology, and gametogenesis in the Manila clam Tapes philippinarum (Adams and Reeve, 1850). Journal of Experimental Marine Biology and Ecology 37: 121–133.

    Article  Google Scholar 

  • Marin, M.G., V. Moschino, M. Deppieri, and L. Lucchetta. 2003. Variations in gross biochemical composition energy value and condition index of T. philippinarum from the Lagoon of Venice. Aquaculture 219 (1-4): 859–871.

    Article  CAS  Google Scholar 

  • Marsh, J.B., and D.B. Weinstein. 1966. Simple charring method for determination of lipid. Journal of Lipid Research 7 (4): 574–576.

    CAS  Google Scholar 

  • Meneghetti, F., V. Moshini, and L. Da Ros. 2004. Gametogenic cycle and variations in oocyte size of Tapes philippinarum from the Lagoon of Venice. Aquaculture 240 (1-4): 473–488.

    Article  Google Scholar 

  • Ministry of Land, Transport and Maritime Affairs, Republic of Korea. 2008. Hebei Spirit oil spill. Reports of marine pollution survey (in Korean).

  • Ministry of Land, Transport and Maritime Affairs, Republic of Korea. 2011. Environmental impact assessment and restoration after the Hebei Spirit oil spill (in Korean).

  • Modassir, Y., and A. Ansari. 2000. Effect of petroleum hydrocarbon on physiological and biochemical parameters in an estuarine clam (Paphia malabarica). Fishery Technology 37: 40–45.

    CAS  Google Scholar 

  • Navarro, E., J.I.P. Iglesias, and A. Larraňaga. 1989. Interannual variation in the reproductive cycle and biochemical composition of the cockle Cerastoderma edule from Mundaca Estuary (Biscay, North Spain). Marine Biology 101 (4): 503–511.

    Article  Google Scholar 

  • Newell, R.I., and B.L. Bayne. 1980. Seasonal changes in the physiology, reproductive condition and carbohydrate content of the cockle Cardium ( = Cerastoderma) edule (bivalve: Cardiidae). Marine Biology 56 (1): 11–19.

    Article  CAS  Google Scholar 

  • Ojea, J., A.J. Pazos, D. Martínez, S. Novoa, J.L. Sánchez, and M. Abad. 2004. Seasonal variation in weight and biochemical composition of the tissues of Rudtapes decussatus in relation to the gametogenic cycle. Aquaculture 238 (1-4): 451–468.

    Article  CAS  Google Scholar 

  • Okumuş, I., and H.P. Stirling. 1998. Seasonal variations in the meat weight, condition index and biochemical composition of mussels (Mytilus edulis L.) in suspended culture in two Scottish Sea lochs. Aquaculture 159 (3-4): 249–261.

    Article  Google Scholar 

  • Olsson, B., B.P. Bradley, M. Gilek, O. Reimer, J.L. Shepard, and M. Tedengren. 2004. Physiological and proteomic responses in Mytilus edulis exposed to PCBs and PAHs extracted from Baltic Sea sediments. Hydrobiologia 514 (1-3): 15–27.

    Article  CAS  Google Scholar 

  • Park, K.I., and K.S. Choi. 2004. Application of enzyme-linked immunosorbent assay for studying of reproduction in the Manila clam Ruditapes philippinarum (Mollusca Bivalvia) I. Quantifying eggs. Aquaculture 241: 667–687.

    Google Scholar 

  • Park, H.J., W.C. Lee, E.J. Choy, K.S. Choi, and C.K. Kang. 2011. Reproductive cycle and gross biochemical composition of the ark shell Scapharca subcrenata (Lischke, 1869) reared on subtidal mudflats in a temperate bay of Korea. Aquaculture 322-323: 149–157.

    Article  CAS  Google Scholar 

  • Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. New York: Peragamon Press.

    Google Scholar 

  • PérezCamacho, A., M. Delgado, M.J. Fernández-Reiriz, and U. Labarta. 2003. Energy balance, gonad development and biochemical composition in the clam Ruditapes decussatus. Marine Ecology Progress Series 258: 133–145.

    Article  Google Scholar 

  • Peteiro, L.G., J.M.F. Babarro, U. Labarta, and M.J. Fernández-Reiriz. 2006. Growth of Mytilus galloprovincialis after the Prestige oil spill. ICES Journal of Marine Science 63: 1005–1013.

    Article  CAS  Google Scholar 

  • Peteiro, L.G., U. Labarta, and M.J. Fernández-Reiriz. 2007. Variability in biochemical components of the mussel (Mytilus galloprovincialis) cultured after Prestige oil spill. Comparative Biochemistry Physiology Part C 145: 588–594.

    Google Scholar 

  • Peterson, C.H., S.D. Rice, J.W. Short, D. Esler, J.L. Bodkin, B.E. Ballachey, and D.B. Irons. 2003. Long-term ecosystem response to the Exxon Valdez oil spill. Science 302 (5653): 2082–2086.

    Article  CAS  Google Scholar 

  • Rice, S.D., J.W. Short, M.G. Carls, A. Moles, and R.B. Spies. 2007. The Exxon Valdez oil spill. In Long-term ecological change in the northern Gulf of Alaska, ed. R.B. Spies, 419–520. Amsterdam: Elsevier.

    Chapter  Google Scholar 

  • Robert, R., G. Trut, and J.L. Laborde. 1993. Growth, reproduction and gross biochemical composition of the Manila clam Ruditapes philippinarum in the Bay of Arcachon, France. Marine Biology 116 (2): 291–299.

    Article  CAS  Google Scholar 

  • Sbrenna, G., and D. Campioni. 1994. Gametogenic and spawning patterns of Manila clams Tapes philippinarum (Bivalvia: Veneroida) in two lagoons of the River Po Delta, Italy. Journal of Shellfish Research 13: 37–46.

    Google Scholar 

  • Smolders, R., L. Bervoets, W. De Coen, and R. Blust. 2004. Cellular energy allocation in zebra mussels exposed along a pollution gradient: Linking cellular effects to higher levels of biological organization. Environmental Pollution 129 (1): 99–112.

    Article  CAS  Google Scholar 

  • Stekoll, M.S., L.E. Clement, and D.G. Shaw. 1980. Sublethal effects of chronic oil exposure on the intertidal clam Macoma balthica. Marine Biology 57 (1): 51–60.

    Article  CAS  Google Scholar 

  • Thomas, H.S. 1993. Oil impacts on marine invertebrate populations and communities. American Zoologist 33: 510–523.

    Article  Google Scholar 

  • Thomas, R.E., C. Brodersen, M.G. Carls, M. Babcock, and S.D. Rice. 1999. Lack of physiological responses to hydrocarbon accumulation by Mytilus trossulus after 3-4 years chronic exposure to spilled Exxon Valdez crude oil in Prince William Sound. Comparative Biochemistry and Physiology Part C 122: 155–163.

    Article  Google Scholar 

  • Toro, B., J.M. Navarro, and H. Palma-Fleming. 2003. Relationship between bioenergetics responses and organic pollutants in the giant mussel, Choromytilus chorus (Mollusca: Mytilidae). Aquatic Toxicology 63 (3): 257–269.

    Article  CAS  Google Scholar 

  • UNEP/OCHA. 2008. Rapid environmental assessment Hebei Spirit oil spill - Republic of Korea, December 2007, 38p. Geneva: A joint Environmental Emergency Response Mission.

    Google Scholar 

  • Widdows, J., T. Bakke, B.L. Bayne, P. Donkin, D.R. Livingstone, D.M. Lowe, M.N. Moore, S.V. Evans, and S.L. Moore. 1982. Responses of Mytilus edulis on exposure to the water-accommodated fraction of North Sea oil. Marine Biology 67 (1): 15–31.

    Article  CAS  Google Scholar 

  • Widdows, J., P. Donkin, and S.V. Evans. 1987. Physiological responses of Mytilus edulis during chronic oil exposure and recovery. Marine Environtal Research 23 (1): 15–32.

    Article  Google Scholar 

Download references

Funding

This research was supported by “Long-term change of structure and function in marine ecosystems of Korea” and “Oil Spill Environmental Impact Assessment and Environmental Restoration: PM55020” funded by the Ministry of Oceans and Fisheries, Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chang-Keun Kang.

Additional information

Communicated by Wen-Xiong Wang

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, H.J., Lee, YJ., Han, E. et al. Effect of the Hebei Spirit Oil Spill on the Condition, Reproduction, and Energy Storage Cycle of the Manila Clam Ruditapes philippinarum on the West Coast of Korea. Estuaries and Coasts 43, 602–614 (2020). https://doi.org/10.1007/s12237-019-00529-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-019-00529-x

Keywords

Navigation