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Estuaries and Coasts

, Volume 35, Issue 3, pp 853–861 | Cite as

Sublethal Effects of Crude Oil on the Community Structure of Estuarine Phytoplankton

  • Kailen Gilde
  • James L. PinckneyEmail author
Article

Abstract

While the ecological impacts of crude oil exposure have been widely studied, its sublethal effects on phytoplankton community structure in salt marsh estuaries have not been well documented. The purpose of this study was to simulate oil spill conditions using a microcosm design to examine short-term (2 day) changes in phytoplankton community composition and total biomass following exposure to crude oil obtained from the Deepwater Horizon oil spill and a mixture of Texas crude oils. Microcosm experiments were performed in situ in North Inlet Estuary near Georgetown, SC. A control and six replicated experimental treatments of crude oil additions at final concentrations of 10, 50, or 100 μl l−1 of either Deepwater Horizon spill oil or the Texas crude mixture were incubated under in situ conditions. Photopigments were analyzed using high-performance liquid chromatography and community composition was determined using ChemTax. Total phytoplankton biomass (as chl a) declined with increasing crude oil concentrations. Prasinophytes, the most abundant microalga in both experiments, showed no response to oil exposure in one experiment and a significant negative response in the other. Diatoms euglenophytes and chlorophytes appeared relatively resistant to oil contamination at the exposure levels used in this study, maintaining or increasing their relative abundance with increasing oil concentrations. Chlorophytes and cyanobacteria increased in relative abundance while cryptophyte abundance decreased with increasing oil concentrations. The results of these experiments suggest that low levels of crude oil exposure may reduce total biomass and alter phytoplankton community composition with possible cascade effects at higher trophic levels in salt marsh estuaries.

Keywords

HPLC ChemTax Bioassay Prasinophytes Diatoms Horizon Maconco spill 

Notes

Acknowledgments

We thank B. Bachmann, E. Kelly, and T. Armstrong for their help with field sampling and HPLC analyses. T. Richardson provided invaluable editorial comments. P. Lillis (USGS) and S. Miles (LSU) provided the crude oil. Funding for this project was obtained through an award to K. Gilde from the Magellan Scholar Undergraduate Research Program, Office of Undergraduate Research, University of South Carolina. This is publication 1640 from the Belle W. Baruch Institute for Marine and Coastal Sciences.

References

  1. Adekunle, I.M., M.R. Ajijo, C.O. Adeofun, and I.T. Omoniyi. 2010. Response of four phytoplankton species found in some sectors of Nigerian coastal waters to crude oil in controlled ecosystem. International Journal of Environmental Research 4: 65–74.Google Scholar
  2. Aksmann, A., and Z. Tukaj. 2008. Intact anthracene inhibits photosynthesis in algal cells: A fluorescence induction study on Chlamydomonas reinhardtii cw92 strain. Chemosphere 74: 26–32.CrossRefGoogle Scholar
  3. Bagchi, M., D. Bagchi, J. Balmoori, X. Ye, and S.J. Stohs. 1998. Naphthalene-induced oxidative stress and DNA damage in cultured macrophage J774A.1 cells. Free Radical Biology and Medicine 25: 137–143.CrossRefGoogle Scholar
  4. Banks, S. 2003. SeaWiFS satellite monitoring of oil spill impact on primary production in the Galapagos Marine Reserve. Marine Pollution Bulletin 47: 325–330.CrossRefGoogle Scholar
  5. Bejarano, A.C., G.T. Chandler, L. He, and B.C. Coull. 2006. Individual to population level effects of South Louisiana crude oil water accommodated hydrocarbon fraction (WAF) on a marine meiobenthic copepod. Journal of Experimental Marine Biology and Ecology 332: 49–59.CrossRefGoogle Scholar
  6. Bopp, S.K., and T. Lettieri. 2007. Gene regulation in the marine diatom Thalassiosira pseudonana upon exposure to polycyclic aromatic hydrocarbons (PAHs). Gene 396: 293–302.CrossRefGoogle Scholar
  7. Dahl, E., M. Laake, K. Tjessem, K. Eberlein, and B. Bohle. 1983. Effects of Ekofisk crude oil on an enclosed planktonic ecosystem. Marine Ecology Progress Series 14: 81–91.CrossRefGoogle Scholar
  8. Diez, I., A. Secilla, A. Santolaria, and J.M. Gorostiaga. 2009. Ecological monitoring of intertidal phytobenthic communities of the Basque Coast (N. Spain) following the Prestige oil spill. Environmental Monitoring and Assessment 159: 555–575.CrossRefGoogle Scholar
  9. Djomo, J.E., A. Dauta, V. Ferrier, J.F. Narbonne, A. Monkiedje, T. Njine, and P. Garrigues. 2004. Toxic effects of some major polyaromatic hydrocarbons found in crude oil and aquatic sediments on Scenedesmus subspicatus. Water Research 38: 1817–1821.CrossRefGoogle Scholar
  10. Echeveste, P., S. Agusti, and J. Dachs. 2010. Cell size dependent toxicity thresholds of polycyclic aromatic hydrocarbons to natural and cultured phytoplankton populations. Environmental Pollution 158: 299–307.CrossRefGoogle Scholar
  11. El-Dib, M.A., H.F. Abou-Waly, and A.H. El-Naby. 2001. Fuel oil effect on the population growth, species diversity, and chlorophyll (a) content of freshwater microalgae. International Journal of Environmental Health Research 11: 189–197.CrossRefGoogle Scholar
  12. El-Sheekh, M.M., A.H. El-Naggar, M.E.H. Osman, and A. Haieder. 2000. Comparative studies on the green algae Chlorella homosphaera and Chlorella vulgaris with respect to oil pollution in the River Nile. Water, Air, and Soil Pollution 124: 187–204.CrossRefGoogle Scholar
  13. Fabregas, J., C. Herrero, and M. Veiga. 1984. Effect of oil and dispersant on growth and chlorophyll a content of the marine microalga Tetraselmis suecica. Applied and Environmental Microbiology 47: 445–447.Google Scholar
  14. Fiala, M., and D. Delille. 1999. Annual changes of microalgae biomass in Antarctic sea ice contaminated by crude oil and diesel fuel. Polar Biology 21: 391–396.CrossRefGoogle Scholar
  15. Fleeger, J.W., K.R. Carman, and R.M. Nisbet. 2003. Indirect effects of contaminants in aquatic ecosystems. The Science of the Total Environment 317: 207–233.CrossRefGoogle Scholar
  16. Gin, K.Y.H., M.D.K. Huda, W.K. Lim, and P. Tkalich. 2001. An oil spill-food chain interaction model for coastal waters. Marine Pollution Bulletin 42: 590–597.CrossRefGoogle Scholar
  17. Gonzalez, J., F.G. Figueiras, M. Aranguren-Gassis, B.G. Crespo, E. Fernandez, X.A.G. Moran, and M. Nieto-Cid. 2009. Effect of a simulated oil spill on natural assemblages of marine phytoplankton enclosed in microcosms. Estuarine, Coastal and Shelf Science 83: 265–276.CrossRefGoogle Scholar
  18. Graham, W.M., R.H. Condon, R.H. Carmichael, I. D'Ambra, H.K. Patterson, L.J. Linn, and F.J. Hernandez Jr. 2010. Oil carbon entered the coastal planktonic food web during the Deepwater Horizon oil spill. Environmental Research Letters 5: 1–6. 045301.CrossRefGoogle Scholar
  19. Hester, M.W., and I.A. Mendelssohn. 2000. Long-term recovery of a Louisiana brackish marsh plant community from oil-spill impact: Vegetation response and mitigating effects of marsh surface elevation. Marine Environmental Research 49: 233–254.CrossRefGoogle Scholar
  20. Hing, L.S., T. Ford, P. Finch, M. Crane, and D. Morritt. 2011. Laboratory stimulation of oil-spill effects on marine phytoplankton. Aquatic Toxicology 103: 32–37.CrossRefGoogle Scholar
  21. Hjorth, M., V.E. Forbes, and I. Dahllof. 2008. Plankton stress responses from PAH exposure and nutrient enrichment. Marine Ecology Progress Series 363: 121–130.CrossRefGoogle Scholar
  22. Jung, S.W., J.S. Park, O.Y. Kown, J. Kang, W.J. Shim, and Y. Kim. 2010. Effects of crude oil on marine microbial communities in short term outdoor microcosms. The Journal of Microbiology 48: 594–600.CrossRefGoogle Scholar
  23. Koshikawa, H., K.Q. Xu, Z.L. Liu, K. Kohata, M. Kawachi, H. Maki, M.Y. Zhu, and M. Watanbe. 2007. Effect of the water-soluble fraction of diesel oil on bacterial and primary production and the trophic transfer to mesozooplankton through a microbial food web in Yangtze estuary, China. Estuarine, Coastal and Shelf Science 71: 68–80.CrossRefGoogle Scholar
  24. Kostka, J.E., O. Prakash, W.A. Overholt, S.J. Green, G. Freyer, A. Canion, J. Delgardio, N. Norton, T.C. Hazen, and M. Huettel. 2011. Bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Applied and Environmental Microbiology 77: 7962–7974.CrossRefGoogle Scholar
  25. Latasa, M. 2007. Improving estimations of phytoplankton class abundances using CHEMTAX. Marine Ecology Progress Series 329: 13–21.CrossRefGoogle Scholar
  26. Leahy, J.G., and R.R. Colwell. 1990. Microbial degradation of hydrocarbons in the environment. Microbiological Reviews 54: 305–315.Google Scholar
  27. Lewitus, A.J., E.T. Koepfler, and J.T. Morris. 1998. Seasonal variation in the regulation of phytoplankton by nitrogen and grazing in a salt-marsh estuary. Limnology and Oceanography 43: 636–646.CrossRefGoogle Scholar
  28. Lewitus, A.J., D.L. White, R.G. Tymowski, M.F. Geesey, S.N. Hymel, and P.A. Noble. 2005. Adapting the CHEMTAX method for assessing phytoplankton taxonomic composition in Southeastern US estuaries. Estuaries 28: 160–172.CrossRefGoogle Scholar
  29. Liu, Y., T. Luan, N. Lu, and C. Lan. 2006. Toxicity of fluoranthene and its biodegradation by Cyclotella caspia alga. Journal of Integrative Plant Biology 48: 169–180.CrossRefGoogle Scholar
  30. Lopez-Rodas, V., D. Carrera-Marinez, E. Salgado, A. Mateos-Sanz, J.C. Baez, and E. Costas. 2009. A fascinating example of microalgal adaptation to extreme crude oil contamination in a natural spill in Arroyo Minero, Rio Negro, Argentina. Anales de la Real Academia Nacional de Farmacia 75: 883–899.Google Scholar
  31. Mackey, M., H. Higgins, D. Mackey, and S. Wright. 1997. CHEMTAX user’s manual: A program for estimating class abundances from chemical markers-application to HPLC measurements of phytoplankton pigments (report 229). Hobart: CSIRO Marine Laboratories.Google Scholar
  32. Mallakin, A., B.J. McConkey, G. Miao, B. McKibben, V. Snieckus, D.G. Dixon, and B.M. Greenburg. 1999. Impacts of structural photomodification on the toxicity of environmental contaminants: Anthracene photooxidation products. Ecotoxicology and Environmental Safety 43: 204–212.CrossRefGoogle Scholar
  33. Miller, M.C., V. Alexander, and R.J. Barsdate. 1978. The effects of oil spills on phytoplankton in an arctic lake and ponds. Arctic 31: 192–218.Google Scholar
  34. Nayar, S., B.P.L. Goh, and L.M. Chou. 2005. Environmental impacts of diesel fuel on bacteria and phytoplankton in a tropical estuary assessed using in situ mesocosms. Ecotoxicology 14: 397–412.CrossRefGoogle Scholar
  35. Ohwada, K., M. Nishimura, M. Wada, H. Nomura, A. Shibata, K. Okamoto, K. Toyoda, A. Yoshida, H. Takada, and M. Yamada. 2003. Study of the effect of water-soluble fractions of heavy-oil on coastal marine organisms using enclosed ecosystems, mesocosms. Marine Pollution Bulletin 47: 78–84.CrossRefGoogle Scholar
  36. Padros, J., E. Pelletier, R. Siron, and D. Delille. 1999. Fate of a new silicone-based oil-treating agent and its effects on marine microbial communities. Environmental Toxicology and Chemistry 18: 819–827.CrossRefGoogle Scholar
  37. Paixao, J.F., I.A. Nascimento, S.A. Pereira, M.B.L. Leite, G.C. Carvalho, J.S.C. Silveira Jr., M. Reboucas, G.R.A. Matias, and I.L.P. Rodrigues. 2007. Estimating the gasoline components and formulations toxicity to microalgae (Tetraselmis chuii) and oyster (Crassotrea rhizophorae) embryos: An approach to minimize environmental pollution risk. Environmental Research 103: 365–374.CrossRefGoogle Scholar
  38. Pinckney, J.L., D.F. Millie, K.E. Howe, H.W. Paerl, and J.P. Hurley. 1996. Flow scintillation counting of 14C labeled microalgal photosynthetic pigments. Journal of Plankton Research 18: 1867–1880.CrossRefGoogle Scholar
  39. Pinckney, J.L., T. Richardson, D. Millie, and H. Paerl. 2001. Application of photopigment biomarkers for quantifying microalgal community composition and in situ growth rates. Organic Geochemistry 32: 585–595.CrossRefGoogle Scholar
  40. Sargian, P., S. Mas, E. Pelletier, and S. Demers. 2007. Multiple stressors on an Antarctic microplankton assemblage: Water soluble crude oil and enhanced UVBR level at Ushuaia (Argentina). Polar Biology 30: 829–841.CrossRefGoogle Scholar
  41. Sikkema, J., J.A.M. de Bont, and B. Poolman. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews 59: 201–222.Google Scholar
  42. Stepaniyan, O.V. 2008. Effects of crude oil on major functional characteristics of macroalgae of the Barents Sea. Russian Journal of Marine Biology 34: 131–134.CrossRefGoogle Scholar
  43. Tas, S., E. Okus, S. Unlu, and H. Altiok. 2011. A study on phytoplankton following ‘Volgoneft-248’ oil spill on the north-eastern coast of the Sea of Marmara. Journal of the Marine Biological Association of the United Kingdom 91: 715–725.CrossRefGoogle Scholar
  44. Varela, M., A. Bode, J. Lorenzo, M.T. Alvarez-Ossorio, A. Miranda, T. Patrocinio, R. Anadon, L. Viesca, N. Rodriguez, L. Valdes, J. Cabal, A. Urrutia, C. Garcia-Soto, M. Rodriguez, X.A. Alvarez-Salgado, and S. Groom. 2006. The effect of the “Prestige” oil spill on the plankton of the N-NW Spanish coast. Marine Pollution Bulletin 53: 272–286.CrossRefGoogle Scholar
  45. Wang, L., and B. Zheng. 2008. Toxic effects of fluoranthene and copper on marine diatom Phaeodactylum tricornutum. Journal of Environmental Sciences 20: 1363–1372.CrossRefGoogle Scholar
  46. Whitehead, A., B. Dubansky, C. Bodinier, T.I. Garcia, S. Miles, C. Pilley, V. Raghunathan, J.L. Roach, N. Walker, R.B. Walter, C.D. Rice, and F. Galvez. 2011. Science applications in the Deepwater Horizon oil spill special feature: Genomic and physiological footprint of the Deepwater Horizon oil spill on resident marsh fishes. Proceedings of the National Academy of Sciences 2011: 1109545108v1-201109545.Google Scholar
  47. Wirth, E.F., M.H. Fulton, G.T. Chandler, P.B. Key, and G.I. Scott. 1998. Toxicity of sediment associated PAHs to the estuarine crustaceans, Palaemonetes pugio and Amphiascus tenuiremis. Bulletin of Environmental Contamination and Toxicology 61: 637–644.CrossRefGoogle Scholar
  48. Wolfe, M.F., H.E. Olsen, K.A. Gasuad, R.S. Tjeerdema, and M.L. Sowby. 1999. Induction of heat shock protein (hsp)60 in Isochrysis galbana exposed to sublethal preparations of dispersant and Prudhoe Bay crude oil. Marine Environmental Research 47: 473–489.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2012

Authors and Affiliations

  1. 1.Marine Science Program and Department of Biological SciencesUniversity of South CarolinaColumbiaUSA

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