Chronic exposure of adults and embryos of Pandalus borealis to oil causes PAH accumulation, initiation of biomarker responses and an increase in larval mortality

Marine Pollution Bulletin

Volumn 60, Issue 11, 2010, Pages 2087-2098

  Bechmann, Renée Katrin ^a   Larsen, Bodil Katrine ^a   Taban, Ingrid Christina ^a   Hellgren, Lars I ^b   Møller, Per ^b   Sanni, Steinar ^a,c  

^a INTERNATIONAL RESEARCH INSTITUTE OF STAVANGER   (Norway)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITY OF STAVANGER   (Norway)

Author keywords

Biomarkers; Embryo; Larvae; Oil water dispersion (OWD); PAH; Pandalus borealis

Indexed keywords

BOREALIS; EMBRYO; LARVAE; OIL-WATER; PAH;

DISPERSIONS; FATTY ACIDS; TISSUE;

BIOMARKERS;

BIOLOGICAL MARKER; DNA; FATTY ACID; NEUTRAL RED; POLYCYCLIC AROMATIC HYDROCARBON;

ADULT; BIOACCUMULATION; BIOASSAY; BIOMARKER; CRUSTACEAN; DNA; EMBRYO; FATTY ACID; MORTALITY; OIL POLLUTION; PAH; POLLUTION EXPOSURE; SURVIVAL;

ARTICLE; BIOACCUMULATION; BLOOD CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DAMAGE; EMBRYO; HATCHING; LARVAL DEVELOPMENT; LARVAL STAGE; LIPID COMPOSITION; LIVER PARENCHYMA; LONG TERM EXPOSURE; LYSOSOME MEMBRANE; MORTALITY; NONHUMAN; SHRIMP; SURVIVAL RATE;

ANIMALS; BIOLOGICAL MARKERS; EMBRYO, NONMAMMALIAN; FATTY ACIDS; LARVA; MORTALITY; PANDALIDAE; POLYCYCLIC HYDROCARBONS, AROMATIC; TISSUE DISTRIBUTION; WATER POLLUTANTS, CHEMICAL;

DECAPODA (CRUSTACEA); PANDALUS BOREALIS;

EID: 78049246331     PISSN: 0025326X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2010.07.010     Document Type: Article

References (60)

1. Anderson, J.W., 1985. Toxicity of Dispersed and Undispersed Prudhoe Bay Crude Oil Fractions to Shrimp, Fish, and their Larvae. Rep. No. 4441. Health and Environmental Sciences Department.
2. Arun S., Rajendran A., Subramanian P. Subcellular/tissue distribution and responses to oil exposure of the cytochrome P450-dependent monooxygenase system and glutathione S-transferase in freshwater prawns (Macrobrachium malcolmsonii, M-lamarrei lamarrei). Ecotoxicology 2006, 15:341-346.
3. Aschan M., Ingvaldsen R. The proceedings of the ECONORTH symposium on ecosystem dynamics in the Norwegian Sea and Barents Sea recruitment of shrimp (Pandalus borealis) in the Barents Sea related to spawning stock and environment. Deep Sea Research Part II: Topical Studies in Oceanography 2008, 56:2012-2022.
4. Bang H.W., Lee W., Kwak I.S. Detecting points as developmental delay based on the life-history development and urosome deformity of the harpacticoid copepod, Tigriopus japonicus sensu lato, following exposure to benzo(a)pyrene. Chemosphere 2009, 76:1435-1439.
5. Batel R., Jaksic Z., Bihari N., Hamer B., Fafandel M., Chauvin C., Schroder H.C., Muller W.E.G., Zahn R.K. A microplate assay for DNA damage determination (fast micromethod) in cell suspensions and solid tissues. Analytical Biochemistry 1999, 270:195-200.
6. Baussant T., Sanni S., Jonsson G., Skadsheim A., Børseth J.F. Bioaccumulation of polycyclic aromatic compounds: 1. Bioconcentration in two marine species and in semipermeable membrane devices during chronic exposure to dispersed crude oil. Environmental Toxicology and Chemistry 2001, 20:1175-1184.
7. Baussant T., Bechmann R.K., Taban I.C., Larsen B.K., Tandberg A.H., Bjørnstad A., Torgrimsen S., Nævdal A., Øysæd K.B., Jonsson G., Sanni S. Enzymatic and cellular responses in relation to body burden of PAHs in bivalve 3 molluscs: a case study with chronic levels of North Sea and Barents Sea dispersed oil. Marine Pollution Bulletin 2009, 58:1796-1807.
8. Bergström B.I. The biology of Pandalus. Advances in Marine Biology 2000, 38:55-245.
9. Brillon S., Lambert Y., Dodson J. Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions. Marine Biology 2005, 147:895-911.
10. Brown R.J., Rundle S.D., Hutchinson T.H., Williams T.D., Jones M.B. A copepod life-cycle test and growth model for interpreting the effects of lindane. Aquatic Toxicology 2003, 63:1-11.
11. Chabot D., Ouellet P. Rearing Pandalus borealis larvae in the laboratory. II. Routine oxygen consumption, maximum oxygen consumption and metabolic scope at three temperatures. Marine Biology 2005, 147:881-894.
12. Douglas G.S., Prince R.C., Butler E.L., Steinhauer W.G. The use of internal chemical indicators in petroleum and refined products to evaluate the extent of biodegradation. Hydrocarbon Bioremediation 1994, 219-236. CRC Press Inc., Boca Raton, FL, US. R.E. Hinchee, B.C. Alleman, R.E. Hoeppel, R.N. Miller (Eds.).
13. Fernley P.W., Moore M.N., Lowe D.M., Donkin P., Evans S. Impact of the Sea Empress oil spill on lysosomal stability in mussel blood cells. Marine Environmental Research 2000, 50:451-455.
14. Fisher W.S., Foss S.S. A simple test for toxicity of number 2 fuel oil and oil dispersants to embryos of grass shrimp Palaemonetes pugio. Marine Pollution Bulletin 1993, 26:385-391.
15. Folch J., Lees M., Stanley G.H.S. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 1957, 226:497-509.
16. Forbes V.E., Palmqvist A., Bach L. The use and misuse of biomarkers in ecotoxicology. Environmental Toxicology and Chemistry 2006, 25:272-280.
17. Geffard O., Geffard A., His E., Budzinski H. Assessment of the bioavailability and toxicity of sediment-associated polycyclic aromatic hydrocarbons and heavy metals applied to Crassostrea gigas embryos and larvae. Marine Pollution Bulletin 2003, 46:481-490.
18. Glas P.S., Courtney L.A., Rayburn J.R., Fisher W.S. Embryonic coat of the grass shrimp Palaemonetes pugio. Biological Bulletin 1997, 192:231-242.
19. Haynes E. Description of larvae of the Northern shrimp, Pandalus borealis, reared in situ in Kachemak Bay, Alaska. Fishery Bulletin 1979, 77:157-173.
20. Heintz R.A., Short J.W., Rice S.D. Sensitivity of fish embryos to weathered crude oil: Part II. Increased mortality of pink salmon (Oncorhynchus gorbuscha) embryos incubating downstream from weathered Exxon Valdez crude oil. Environmental Toxicology and Chemistry 1999, 18:494-503.
21. Hylland K., Tollefsen K.E., Ruus A., Jonsson G., Sundt R.C., Sanni S., Utvik T.I.R., Johnsen S., Nilssen I., Pinturier L., Balk L., Barsiene J., Marigomez I., Feist S.W., Børseth J.F. Water column monitoring near oil installations in the North Sea 2001-2004. Marine Pollution Bulletin 2008, 56:414-429.
22. Jaksic Z., Batel R. DNA integrity determination in marine invertebrates by fast micromethod (R). Aquatic Toxicology 2003, 65:361-376.
23. Jaksic Z., Batel R., Bihari N., Micic M., Zahn R.K. Adriatic coast as a microcosm for global genotoxic marine contamination - a long-term field study. Marine Pollution Bulletin 2005, 50:1314-1327.
24. James M.O., Boyle S.M. Cytochromes P450 in crustacea. Comparative Biochemistry and Physiology C-Toxicology and Pharmacology 1998, 121:157-172.
25. Jonsson G., Bechmann R.K., Bamber S.D., Baussant T. Bioconcentration, biotransformation, and elimination of polycyclic aromatic hydrocarbons in sheepshead minnows (Cyprinodon variegatus) exposed to contaminated seawater. Environmental Toxicology and Chemistry 2004, 23:1538-1548.
26. Larsen B.K., Buffagni M., Moltu U.E., Baussant T., Skadsheim A., Bechmann R.K., Sundt R., Beyer J., Borseth J.F., Aas E., Bjørnbom E., Bracco L., Pinturier L., Sanni S. Biosea Joint Industry project - development of a global biomonitoring tool for the petroleum industry offshore. Marine Environmental Research 2006, 62:S407-S408.
27. Lavarias S., Heras H., Pollero R.J. Toxicity, uptake, and release of the water-soluble fraction of crude oil in different developing stages of the prawn Macrobrachium borellii. Archives of Environmental Contamination and Toxicology 2004, 47:215-222.
28. Levin L., Caswell H., Bridges T., DiBacco C., Cabrera D., Plaia G. Demographic responses of estuarine polychaetes to pollutants: life table response experiments. Ecological Applications 1996, 6:1295-1313.
29. Lewis C., Pook C., Galloway T. Reproductive toxicity of the water accommodated fraction (WAF) of crude oil in the polychaetes Arenicola marina (L.) and Nereis virens (Sars). Aquatic Toxicology 2008, 90:73-81.
30. Livingstone D.R. The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comparative Biochemistry and Physiology a-Molecular and Integrative Physiology 1998, 120:43-49.
31. Lowe D.M., Fossato V.U., Depledge M.H. Contaminant-induced lysosomal membrane damage in blood cells of mussels Mytilus galloprovincialis from the Venice Lagoon: an in vitro study. Marine Ecology-Progress Series 1995, 129:189-196.
32. Martins L.K.P., Nascimento I.A., Fillmann G., King R., Evangelista A.J.A., Readman J.W., Depledge M.H. Lysosomal responses as a diagnostic tool for the detection of chronic petroleum pollution at Todos os Santos Bay, Brazil. Environmental Research 2005, 99:387-396.
33. Mathews C.P., Kedidi S., Fita N.I., Alyahya A., Alrasheed K. Preliminary assessment of the effects of the 1991 Gulf-War on Saudi-Arabian prawn stocks. Marine Pollution Bulletin 1993, 27:251-271.
34. Misra C.K., Das B.K., Pradhan J., Pattnaik P., Sethi S., Mukherjee S.C. Changes in lysosomal enzyme activity and protection against vibrio infection in Macrobrachium rosenbergii (De Man) post larvae after bath immunostimulation with beta-glucan. Fish and Shellfish Immunology 2004, 17:389-395.
35. Moles A. Sensitivity of ten aquatic species to long-term crude oil exposure. Bulletin of Environmental Contamination and Toxicology 1998, 61:102-107.
36. Moles A. Parasitism, feeding rate, and hydrocarbon uptake of pink shrimp Pandalus borealis fed a crude oil contaminated diet. Bulletin of Environmental Contamination and Toxicology 1999, 62:259-265.
37. Moore M.N., Allen J.I., McVeigh A. Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Marine Environmental Research 2006, 61:278-304.
38. Moore, M.N., Kohler, A., Lowe, D., Viarengo, A., 2008. Lysosomes and autophagy in aquatic animals. In: Autophagy: Lower Eukaryotes and Non-Mammalian Systems. Methods in Enzymology, vol. 451, pp. 581-620.
39. Muller H., Hellgren L.I., Olsen E., Skrede A. Lipids rich in phosphatidylethanolamine from natural gas-utilizing bacteria reduce plasma cholesterol and classes of phospholipids: a comparison with soybean oil. Lipids 2004, 39:833-841.
40. Ouellet P., Chabot D. Rearing Pandalus borealis (Kröyer) larvae in the laboratory. Marine Biology 2005, 147:869-880.
41. Ouellet P., Taggart C.T., Frank K.T. Lipid condition and survival in shrimp (Pandalus borealis) larvae. Canadian Journal of Fisheries and Aquatic Sciences 1992, 49:368-378.
42. Pedersen S., Storm L. Northern shrimp (Pandalus borealis) recruitment in West Greenland waters Part II. Lipid classes and fatty acids in Pandalus shrimp larvae: implications for survival. Expectations and trophic relationships. Journal of Northwest Atlantic Fishery Science 2002, 30:47-60.
43. Pillai M.C., Vines C.A., Wikramanayake A.H., Cherr G.N. Polycyclic aromatic hydrocarbons disrupt axial development in sea urchin embryos through a beta-catenin dependent pathway. Toxicology 2003, 186:93-108.
44. Price A.R.G. Impact of the 1991 Gulf War on the coastal environment and ecosystems: current status and future prospects. Environment International 1998, 24:91-96.
45. Price A.R.G., Mathews C.P., Ingle R.W., Alrasheed K. Abundance of zooplankton and Penaeid shrimp larvae in the Western Gulf - Analysis of prewar (1991) and postwar data. Marine Pollution Bulletin 1993, 27:273-278.
46. Rayburn J.R., Fisher W.S. Developmental toxicity of three carrier solvents using embryos of the grass shrimp, Palaemonetes pugio. Archives of Environmental Contamination and Toxicology 1997, 33:217-221.
47. Rust A.J., Burgess R.M., Brownawell B.J., McElroy A.E. Relationship between metabolism and bioaccumulation of benzo[a]pyrene in benthic invertebrates. Environmental Toxicology and Chemistry 2004, 23:2587-2593.
48. Rye H., Johansen O., Reed M., Ekrol N., Xiong D.Q. Exposure of fish larvae to hydrocarbon concentration fields generated by subsurface blowouts. Spill Science and Technology Bulletin 2000, 6:113-123.
49. Sanborn H.R., Malins D.C. The disposition of aromatic hydrocarbons in adult spot shrimp (Pandalus platyceros) and the formation of metabolites of naphthalene in adult and larval spot shrimp. Xenobiotica 1980, 10:193-200.
50. Sanchez F., Velasco F., Cartes J.E., Olaso I., Preciado I., Fanelli E., Serrano A., Gutierrez-Zabala J.L. Monitoring the Prestige oil spill impacts on some key species of the Northern Iberian shelf. Marine Pollution Bulletin 2006, 53:332-349.
51. Sanni S., Øysæd K.B., Høivangli V., Gaudebert B. A continuous flow system (CFS) for chronic exposure of aquatic organisms. Marine Environmental Research 1998, 46:97-101.
52. Skadsheim A., Sanni S., Pinturier L., Moltu U.-E., Buffagni M., Bracco L. Assessing and monitoring local and long-range-transported hydrocarbons as potential stressors to fish stocks. Deep Sea Research Part II: Topical Studies in Oceanography 2009, 56:2037-2043.
53. Smit M.G.D., Bechmann R.K., Hendriks A.J., Skadsheim A., Larsen B.K., Baussant T., Bamber S., Sanni S. Relating biomarkers to whole-organism effects using species sensitivity distributions: a pilot study for marine species exposed to oil. Environmental Toxicology and Chemistry 2009, 28:1104-1109.
54. Stickle, W.B., Kapper, M.A., Shirley, T.C., Carls, M.G., Rice, S.D., 1987. Bioenergetics and tolerance of the pink shrimp (Pandalus borealis) during long-term exposure to the water-soluble fraction and oiled sediment from Cook Inlet crude oil. In: Vernberg, W.B., Calabrese, A., Thurberg, F.P., Vernberg, F.J. (Eds.), Pollution Physiology of Estuarine Organisms, Belle W. Baruch Libr. Mar. Sci. 17. Univ. S. C. Press, Columbia, pp. 87-106.
55. Sung H.H., Kou G.H., Song Y.L. Vibriosis resistance induced by glucan treatment in Tiger shrimp (Penaeus monodon). Fish Pathology 1994, 29:11-17.
56. Taban I.C., Bechmann R.K., Torgrimsen S., Baussant T., Sanni S. Detection of DNA damage in mussels and sea urchins exposed to crude oil using comet assay. Marine Environmental Research 2004, 58:701-705.
57. Taban I.C., Bechmann R.K., Torgrimsen S., Sundt R., Bjornstad A., Larsen B.K., Andersen O.K. DNA damage in mussels following exposure to three potential endocrine disruptors using the comet assay and the alkaline unwinding assay. Marine Environmental Research 2008, 66:65.
58. Wedderburn J., McFadzen I., Sanger R.C., Beesley A., Heath C., Hornsby M., Lowe D. The field application of cellular and physiological biomarkers, in the mussel Mytilus edulis, in conjunction with early life stage bioassays and adult histopathology. Marine Pollution Bulletin 2000, 40:257-267.
59. Wehrtmann I.S., Graeve M. Lipid composition and utilization in developing eggs of two tropical marine caridean shrimps (Decapoda: Caridea: Alpheidae, Palaemonidae). Comparative Biochemistry and Physiology B-Biochemistry and Molecular Biology 1998, 121:457-463.
60. Worboys M.A., Leung K.M.Y., Grist E.P.M., Crane M. Time should be considered in developmental ecotoxicity test. Marine Pollution Bulletin 2002, 45:92-99.