Abstract
The 2010 explosion of the Deepwater Horizon (DWH) oil rig generated the largest marine oil spill in US history with millions of barrels of crude oil released in the Gulf of Mexico (GoM). The eastern oyster, Crassostrea virginica, is an ecologically and economically important species in the northern GoM. Due to its biological characteristics (sessile, filter feeding), juvenile oysters may have been affected. This study investigated the effects of surface-collected DWH oil prepared as high-energy water-accommodated fraction (HEWAF) on the survival of 2-month-old oyster spat, and evaluated the potential impacts of HEWAF on particle clearance rate and spat tissue. Exposure of oysters to a range of oil/HEWAF (0–7–66–147–908–3450 μg tPAH50 (sum of 50 polycyclic aromatic hydrocarbons) L−1) resulted in non-dose-dependent mortalities and reduced clearance rates of algal food (Tisochrysis lutea). A morphometric study of the digestive tubules (DGTs) indicated a dose-dependent response to oil exposure on lumen dilation, on epithelium thinning of the DGT, and a significant change in DGT synchrony (LOEC = 66 μg tPAH50 L−1). This finding suggests that structural changes occurred in the digestive gland of exposed oysters most likely due to an oil-related stress. In addition, histological observations showed that tissues in contact with HEWAF (gills, palp, connective tissue, digestive gland) were adversely impacted at ≥ 7 μg tPAH50 L−1, and exhibited pathological symptoms typical of an inflammatory response (e.g., hemocyte diapedesis and infiltration, syncytia, epithelium sloughing).
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References
Achten C, Andersson JT (2015) Overview of polycyclic aromatic compounds (PAC). Polycycl Aromat Compd 35(2–4):177–186
Akberali HB, Trueman ER (1985) Effects of environmental stress on marine bivalve molluscs. Adv Mar Biol 22:101–198
Allan SE, Smith BW, Anderson KA (2012) Impact of the Deepwater Horizon oil spill on bioavailable polycyclic aromatic hydrocarbons in Gulf of Mexico coastal waters. Environ Sci Technol 46:2033–2039
Alves de Almeida E, Celso Dias Bainy A, Paula de Melo Loureiro A, Regina Martinez G, Miyamoto S, Onuki J, Di Mascio P (2007) Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: antioxidants, lipid peroxidation and DNA damage. Comp Biochem Physiol A Mol Integr Physiol 146(4):588–600
Anderson RS (1987) Polykaryon formation by Mercenaria mercenaria hemocytes. Biol Bull 172(2):236–245
Axiak V, George JJ (1987) Bioenergetic responses of the marine bivalve Venus verrucosa on long-term exposure to petroleum hydrocarbons. Mar Environ Res 23(1):33–47
Axiak V, George JJ, Moore MN (1988) Petroleum hydrocarbons in the marine bivalve Venus verrucosa: accumulation and cellular responses. Mar Biol 97(2):225–230
Barron MG, Podrabsky T, Ogle S, Ricker RW (1999) Are aromatic hydrocarbons the primary determinant of petroleum toxicity to aquatic organisms? Aquat Toxicol 46(3):253–268
Barron MG, Carls MG, Short JW, Rice SD (2003) Photo-enhanced toxicity of aqueous phase and chemically dispersed weathered Alaska North Slope crude oil to Pacific herring eggs and larvae. Environ Toxicol Chem 22(3):650–660
Barszcz C, Yevich PP, Brown LR, Yarborough JD, Minchew CD (1977) Chronic effects of three crude oils on oysters suspended in estuarine ponds. J Environ Pathol Toxicol 1:879–895
Berthou F, Balouet G, Bodennec G, Marchand M (1987) The occurrence of hydrocarbons and histopathological abnormalities in oysters for seven years following the wreck of the Amoco Cadiz in Brittany (France). Mar Environ Res 23(2):103–133
Boesch D (2014) Expert report prepared on behalf of the United States (TREX-013183). U.S. v. BP Exploration & Production, Inc. 12
Cajaraville M, Díez G, Larrea P, Marigómez JA, Angulo E (1989) Planimetric parameters of the digestive tubules of Mytilus edulis: a sensitive tool for monitoring petroleum hydrocarbon toxicity. Seminario Internacional do mexillon. Toxa, O Grove (Spain). 6-10 Nov 1989
Cajaraville MP, Uranga JA, Angulo E (1992) Comparative effects of the water accommodated fraction of three oils on mussels—3. Quantitative histochemistry of enzymes related to the detoxication metabolism. Comp Biochem Physiol C Comp Pharmacol 103(2):369–377
Calabrese A, MacInnes JR, Nelson DA, Greig RA, Yevich PP (1984) Effects of long-term exposure to silver or copper on growth, bioaccumulation and histopathology in the blue mussel Mytilus edulis. Mar Environ Res 11(4):253–274
Capuzzo JM (1996) The bioaccumulation and biological effects of lipophilic organic contaminants. The Eastern Oyster Crassostrea virginica MD Sea Grant Publication, pp 539–557
Carls MG, Holland L, Larsen M, Collier TK, Scholz NL, Incardona JP (2008) Fish embryos are damaged by dissolved PAHs, not oil particles. Aquat Toxicol 88(2):121–127
Carriger J, Barron MG (2011) Minimizing risks from spilled oil to ecosystem services using influence diagrams: the Deepwater Horizon spill response. Environ Sci Technol 45:7631–7639
Coen LD, Brumbaugh RD, Bushek D, Grizzle R, Luckenbach MW, Posey MH, Powers SP, Tolley S (2007) Ecosystem services related to oyster restoration. Mar Ecol Prog Ser 341:303–307
Coughlan J (1969) The estimation of filtering rate from the clearance of suspensions. Mar Biol 2:356–358
Di Giulio RT, Washburn PC, Wenning RJ, Winston GW, Jewell CS (1989) Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ Toxicol Chem 8(12):1103–1123
Domingos FV, Azevedo M, Silva MD, Randi MAF, Freire CA, de Assis HS, Ribeiro CO (2007) Multibiomarker assessment of three Brazilian estuaries using oysters as bioindicators. Environ Res 105(3):350–363
Donkin P, Widdows J (1990) Quantitative structure-activity relationships in aquatic invertebrate toxicology. Rev Aquat Sci 2(3, 4):375–398
Poole AR, Howell JI, Lucy JA (1970) Lysolecithin and cell fusion. Nature 227(5260):810–814. https://doi.org/10.1038/227810a0
Downs CA, Shigenaka G, Fauth JE, Robinson CE, Huang A (2002) Cellular physiological assessment of bivalves after chronic exposure to spilled Exxon Valdez crude oil using a novel molecular diagnostic biotechnology. Environ Sci Technol 36(13):2987–2993
Environmental Response Management Application (2015) Deepwater gulf response. National Oceanic and Atmospheric Administration. Available: http://response.restoration.noaa.gov/maps-and-spatial-data/environmental-response-management-application-erma/erma-gulf-response.html. Accessed 30 Jul 2015
Farrington JW, Goldberg ED, Risebrough RW, Martin JH, Bowen VT (1983) US “Mussel Watch” 1976-1978: an overview of the trace-metal, DDE, PCB, hydrocarbon and artificial radionuclide data. Environ Sci Technol 17(8):490–496
Feng SY (1966) Experimental bacterial infections in the oyster Crassostrea virginica. J Invertebr Pathol 8(4):505–511
Fisher WS, Tamplin M (1988) Environmental influence on activities and foreign-particle binding by hemocytes of American oysters, Crassostrea virginica. Can J Fish Aquat Sci 45(7):1309–1315
Forth HP, Mitchelmore CL, Morris JM, Lay CR, Lipton J (2017) Characterization of dissolved and particulate phases of water accommodated fractions used to conduct aquatic toxicity testing in support of the Deepwater Horizon natural resource damage assessment. Environ Toxicol Chem 36:1460–1472. https://doi.org/10.1002/etc.3803
Gainey LF, Shumway SE (1991) The physiological effect of Aureococcus anophagefferens (“brown tide”) on the lateral cilia of bivalve mollusks. Biol Bull 181(2):298–306
Galimany E, Sunila I, Hégaret H, Ramón M, Wikfors GH (2008) Experimental exposure of the blue mussel (Mytilus edulis) to the toxic dinoflagellate, Alexandrium fundyense: histopathology, immune responses, and recovery. Harmful Algae 7(5):702–711
Galtsoff PS, Prytherch HF, Smith RO, Koehring V (1935) Effects of crude oil pollution on oysters in Louisiana waters. US Government Printing Office, Washington, D.C.
Gilewicz M, Guillaume JR, Carles D, Leveau M, Bertrand JC (1984) Effects of petroleum hydrocarbons on the cytochrome P450 content of the mollusk bivalve Mytilus galloprovincialis. Mar Biol 80(2):155–159
Graham WM, Condon RH, Carmichael RH, D’Ambra I, Patterson HK, Linn LJ, Hernandez FJ Jr (2010) Oil carbon entered the coastal planktonic food web during the Deepwater Horizon oil spill. Environ Res Lett 5(4):045301
Hansen BH, Altin D, Olsen AJ, Nordtug T (2012) Acute toxicity of naturally and chemically dispersed oil on the filter-feeding copepod Calanus finmarchicus. Ecotoxicol Environ Saf 86:38–46
Hawthorne SB, Miller DJ, Kreitinger JP (2006) Measurement of total polycyclic aromatic hydrocarbon concentrations in sediments and toxic units used for estimating risk to benthic invertebrates at manufactured gas plant sites. Environ Toxicol Chem 25(1):287–296
Howard DW, Lewis EJ, Keller BJ, Smith CS (2004) Histological techniques for marine bivalve mollusks and crustaceans. NOAA Technical Memorandum NOS NCCOS 5, 218 pp
Huerta L, López-Balderas N, Rivera-Toledo E, Sandoval G, Gȑmez-Icazbalceta G, Villarreal C, Larralde C (2009) HIV-envelope-dependent cell-cell fusion: quantitative studies. Sci World J 9:746–763
Kim Y, Ashton-Alcox KA, Powell EN (2006) Histological techniques for marine bivalve molluscs: update. NOAA/National Centers for Coastal Ocean Science, Silver Spring 64pp. (NOAA Technical Memorandum NOS NCCOS, 27)
Lee RF, Gardner WS, Anderson JW, Blaylock JW, Barwell-Clarke J (1978) Fate of polycyclic aromatic hydrocarbons in controlled ecosystem enclosures. Environ Sci Technol 12(7):832–838
Lewis MR (1925) The formation of macrophages, epithelioid cells and giant cells from leucocytes in incubated blood carnegie institution. Am J Pathol 1(1):91–100.1
Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666
Livingstone DR, Garcia Martinez P, Winston GW (1989) Menadione-stimulated oxyradical formation in digestive gland musomes of the common mussel, Mytilus edulis L. Aquat Toxicol 15(3):213–236
Lowe DM, Moore MN, Clarke KR (1981) Effects of oil on digestive cells in mussels: quantitative alterations in cellular and lysosomal structure. Aquat Toxicol 1(3):213–226
Luna-Acosta A, Kanan R, Le Floch S, Huet V, Pineau P, Bustamante P, Thomas-Guyon H (2011) Enhanced immunological and detoxification responses in Pacific oysters, Crassostrea gigas, exposed to chemically dispersed oil. Water Res 45(14):4103–4118
Luna-Acosta A, Bustamante P, Thomas-Guyon H, Zaldibar B, Izagirre U, Marigómez I (2017) Integrative biomarker assessment of the effects of chemically and mechanically dispersed crude oil in Pacific oysters, Crassostrea gigas. Sci Total Environ 598:713–721
Mariano M, Spector WG (1974) The formation and properties of macrophage polykaryons (inflammatory giant cells). J Pathol 113(1):1–19
Moore MN (1985) Cellular responses to pollutants. Mar Pollut Bull 16(4):134–139
Morton BS (1977) The tidal rhythm of feeding and digestion in the pacific oyster, Crassostrea gigas (Thunberg). J Exp Mar Biol Ecol 26(2):135–151
National Commission on the BP Deepwater Horizon oil spill and offshore drilling (2010) Stopping the spill: the five-month effort to kill the Macondo well. Draft. Staff working Paper No. 6. November 22. Available: http://permanent.access.gpo.gov/gpo2428/Containment%20Working%20Paper%2011%2022%2010.pdf. Accessed 7 Jul 2015
National Marine Fisheries Service, NMFS (2012). Annual commercial landing statistics, Fisheries Statistics. Available at http://www.st.nmfs.noaa.gov/st1/commercial/landings/annual_landings.html. Last consulted in July 2014
National Research Council, NRC (2003) Oil in the sea III: inputs, fates, and effects. National Academy, Washington, DC. https://doi.org/10.17226/10388
Neff JM (1985) “Polycyclic aromatic hydrocarbons.” Fundamentals of aquatic toxicology: methods and applications. Hemisphere Publishing Corporation, Washington, DC, pp 416–454
Neff JM, Anderson JW (1981) Response of marine animals to petroleum and specific petroleum hydrocarbons. New York, Applied Science Pub. Halsted Press
Neff JM, Haensly WE (1982) Long-term impact of the Amoco Cadiz crude oil spill on oysters Crassostrea gigas and plaice Pleuronectes platessa from Aber Benoit and Aber Wrac’h, Brittany, France. Ecological Study of the AMOCO Cadiz Oil Spill 1982. pp 269–327
Neff JM, Stubblefield WA (1995) Chemical and toxicological evaluation of water quality following the Exxon Valdez oil spill. ASTM Special Technical Publication (1219), pp 141–177
Newell RI (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23(1):51–62
Nixon Z, Zengel S, Michel J (2015) NOAA technical report: categorization of shoreline oiling from the Deepwater Horizon oil spill. https://pub-dwhdatadiver.orr.noaa.gov/dwh-ar-documents/901/DWH-AR0270684.pdf
O’Connor TP, Lauenstein GG (2006) Trends in chemical concentrations in mussels and oysters collected along the US coast: update to 2003. Mar Environ Res 62(4):261–285
Owen G (1973) Feeding and digestion in the bivalvia. Adv Comp Physiol Biochem 5:1–35
Pelletier MC, Burgess RM, Ho KT, Kuhn A, McKinney RA, Ryba SA (1997) Phototoxicity of individual polycyclic aromatic hydrocarbons and petroleum to marine invertebrate larvae and juveniles. Environ Toxicol Chem 16(10):2100–2199
Powers SP, Grabowski JH, Roman H, Geggel A, Rouhani S, Oehrig J, Baker M (2015) Consequences of large scale hydrographic alteration during the Deepwater Horizon oil spill on subtidal oyster populations. Technical report, September 9, 2015. DWH-AR0270347
Sami S, Faisal M, Huggett RJ (1992) Alterations in cytometric characteristics of hemocytes from the American oyster Crassostrea virginica exposed to a polycyclic aromatic hydrocarbon (PAH) contaminated environment. Mar Biol 113(2):247–252
Supan J (1983) Evaluation of a leased oyster bottom in Mississippi Sound. Gulf Res Rep 7(3):261–266
U.S. District Court (2014) In re: Oil spill by the oil rig “Deepwater Horizon” in the Gulf of Mexico, on April 20, 2010, No. MDL 2179, Section 7 (Revised September 9, 2014) (“Findings of fact and conclusions of law: phase one trial”), Figure 1. United States District Court for the Eastern District of Louisiana
U.S. District Court (2015) In re: Oil spill by the oil rig “Deepwater Horizon” in the Gulf of Mexico, on April 20, 2010, No. MDL 2179, 2015 WL 225421 (La. E.D. Jan. 15, 2015) (“Findings of fact and conclusions of law: phase two trial”). United States District Court for the Eastern District of Louisiana
US Environmental Protection Agency (1986). SW-846 manual for waste testing, Vol. 1B and 1C. Washington, DC, 8270D pp 1–72
Vignier J, Donaghy L, Soudant P, Chu FLE, Morris JM, Carney MW, Lay C, Krasnec M, Robert R, Volety AK (2015) Impacts of Deepwater Horizon oil and associated dispersant on early development of the eastern oyster, Crassostrea virginica. Mar Pollut Bull 100:426–437 https://doi.org/10.1016/j.marpolbul.2015.08.011
Vignier J, Soudant P, Chu FLE, Morris JM, Carney LC, Krasnec MO, Robert R, Volety AK (2016) Lethal and sublethal effects of Deepwater Horizon slick oil and dispersant on oyster (Crassostrea virginica) larvae. Mar Environ Res 120:20–31
Wells HW (1961) The fauna of oyster beds, with special reference to the salinity factor. Ecol Monogr 31(3):239–266
Widdows J, Bakke T, Bayne BL, Donkin P, Livingstone DR, Lowe DM, Moore MN, Evans SV, Moore SL (1982) Responses of Mytilus edulis on exposure to the water-accommodated fraction of North Sea oil. Mar Biol 67(1):15–31
Wikfors GH, Smolowitz RM (1995) Experimental and histological studies of four life-history stages of the eastern oyster, Crassostrea virginica, exposed to a cultured strain of the dinoflagellate Prorocentrum minimum. Biol Bull 188(3):313–328
Winstead JT (1995) Digestive tubule atrophy in eastern oysters, Crassostrea virginica (Gmelin, 1791), exposed to salinity and starvation stress. J Shellfish Res 14(1):105–112
Yamuna A, Kabila V, Geraldine P (1996) Biochemical and histological alterations in the prawn Macrobrachium lamerrei following exposure to automobile discharge. GeoJournal 40(1–2):233–237
Acknowledgements
The findings and conclusions presented in this study are those of the authors and do not necessarily represent the view of National Oceanic and Atmospheric Administration (NOAA) or of any other Trustees for the BP/Deepwater Horizon NRDA. We would like to thank the Abt Associates, particularly Michelle Krasnec and Jeffrey Morris, for their contributions. We thank Scott Rikard at the Auburn University Shellfish Laboratory, Dauphin Island, AL, for providing the oyster spat. We are also grateful to Inke Sunila at the Connecticut Department of Agriculture for her unlimited knowledge on shellfish histopathology and to Hélène Hégaret for a review of an earlier version of the manuscript. Finally, this study would not have been possible without the technical assistance from the graduate students and staff at the Vester Field Station, especially Gaelle Richard, Molly Rybovich, Nicole Martin, Emily Standen-Nickols, and Audrey Barbe.
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This work was supported by funds provided as part of the Natural Resource Damage Assessment (NRDA) for the Deepwater Horizon oil spill.
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Initial concentrations, expressed in μg L−1, for the 50 PAH analytes (parent and alkyl homologs) measured in the fresh stock solutions of HEWAF (oil loading rate of 2 g L−1) throughout the 10 day-exposure of oyster spat. Generalized subclasses are divided by dotted lines and noted on the figure (GIF 105 kb)
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Vignier, J., Rolton, A., Soudant, P. et al. Evaluation of toxicity of Deepwater Horizon slick oil on spat of the oyster Crassostrea virginica . Environ Sci Pollut Res 25, 1176–1190 (2018). https://doi.org/10.1007/s11356-017-0476-2
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DOI: https://doi.org/10.1007/s11356-017-0476-2