Abstract
Arctic shipping and oil exploration are expected to increase, as sea ice extent is reduced. This enhances the risk for accidental oil spills throughout the Arctic, which emphasises the need to quantify potential consequences to the marine ecosystem and to evaluate risk and choose appropriate remediation methods. This study investigated the sensitivity of Arctic marine plankton to the water accommodated fraction (WAF) of heavy fuel oil. Arctic marine phytoplankton and copepods (Calanus finmarchicus) were exposed to three WAF concentrations corresponding to total hydrocarbon contents of 0.07 mg l−1, 0.28 mg l−1 and 0.55 mg l−1. Additionally, the potential phototoxic effects of exposing the WAF to sunlight, including the UV spectrum, were tested. The study determined sub-lethal effects of WAF exposure on rates of key ecosystem processes: primary production of phytoplankton and grazing (faecal pellet production) of copepods. Both phytoplankton and copepods responded negatively to WAF exposure. Biomass specific primary production was reduced by 6, 52 and 73% and faecal pellet production by 18, 51 and 86% with increasing WAF concentrations compared to controls. The phototoxic effect reduced primary production in the two highest WAF concentration treatments by 71 and 91%, respectively. This experiment contributes to the limited knowledge of acute sub-lethal effects of potential oil spills to the Arctic pelagic food web.
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Agersted MD, Møller EF, Gustavson K (2018) Bioaccumulation of oil compounds in the high-Arctic copepod Calanus hyperboreus. Aquat Toxicol 195:8 14. https://doi.org/10.1016/j.aquatox.2017.12.001
Ardyna M, Babin M, Gosselin M et al. (2013) Parameterization of vertical chlorophyll a in the Arctic Ocean: Impact of the subsurface chlorophyll maximum on regional, seasonal, and annual primary production estimates. Biogeosciences 10:4383 4404. https://doi.org/10.5194/bg-10-4383-2013
Barron MG, Carls MG, Short JW, Rice SD (2003) Photoenhanced toxicity of aqueous phase and chemically dispersed weathered Alaska North Slope crude oil to Pacific herring eggs and larvae. Environ Toxicol Chem 22:650 660. https://doi.org/10.1002/etc.5620220326
Bouchard JN, Longhi ML, Roy S et al. (2008) Interaction of nitrogen status and UVB sensitivity in a temperate phytoplankton assemblage. J Exp Mar Bio Ecol 359:67 76. https://doi.org/10.1016/J.JEMBE.2008.02.022
Brandvik J, Faksness L-G (2009) Weathering processes in Arctic oil spills: Meso-scale experiments with different ice conditions. Cold Reg Sci Technol 55:160 166. https://doi.org/10.1016/j.coldregions.2008.06.006
Brussaard CPD, Peperzak L, Beggah S et al. (2016) Immediate ecotoxicological effects of short-lived oil spills on marine biota. Nat Commun 7: https://doi.org/10.1038/ncomms11206
Daling PS, Singsaas I, Reed M, Hansen O (2002) Experiences in dispersant treatment of experimental oil spills. Spill Sci Technol Bull 7:201 213. https://doi.org/10.1016/S1353-2561(02)00061-0
Daling PS, Strøm T (1999) Weathering of oils at sea: Model/Field data comparisons. Spill Sci Technol Bull 5:63 74. https://doi.org/10.1016/S1353-2561(98)00051-6
Duesterloh S, Short* JW, Barron MG (2002) Photoenhanced Toxicity of Weathered Alaska North Slope Crude Oil to the Calanoid Copepods Calanus marshallae and Metridia okhotensis. Environ Sci Technol 36:3953 3959. https://doi.org/10.1021/ES020685Y
Eguíluz VM, Fernández-Gracia J, Irigoien X, Duarte CM (2016) A quantitative assessment of Arctic shipping in 2010—2014. Sci Rep 6: https://doi.org/10.1038/srep30682
Finch BE, Marzooghi S, Di Toro DM, Stubblefield WA (2017) Phototoxic potential of undispersed and dispersed fresh and weathered Macondo crude oils to Gulf of Mexico Marine Organisms. Environ Toxicol Chem 36:2640 2650. https://doi.org/10.1002/etc.3808
Fistarol G, Legrand C, Granéli E (2005) Allelopathic effect on a nutrient-limited phytoplankton species. Aquat Microb Ecol 41:153 161. https://doi.org/10.3354/ame041153
Fritt-Rasmussen J, Wegeberg S, Gustavson K et al. (2018) Heavy Fuel Oil (HFO) A review of fate and behaviour of HFO spills in cold seawater, including biodegradation, environmental effects and oil spill response. The Nordic Council of Ministers, Copenhagen
Gardiner WW, Word JQ, Word JD et al. (2013) The acute toxicity of chemically and physically dispersed crude oil to key arctic species under arctic conditions during the open water season. Environ Toxicol Chem 32:2284 2300. https://doi.org/10.1002/etc.2307
Garrett RM, Pickering IJ, Copper E, Haith A, Prince RC (1998) Photooxidation of crude oils. Environ Sci Technol 32:3719 3723. https://doi.org/10.1021/ES980201R
Grenvald JC, Nielsen TG, Hjorth M (2013) Effects of pyrene exposure and temperature on early development of two co-existing Arctic copepods. Ecotoxicology 22:184 198. https://doi.org/10.1007/s10646-012-1016-y
Hansen BH, Nordtug T, Altin D et al. (2009) Gene Expression of GST and CYP330A1 in Lipid-Rich and Lipid-Poor Female Calanus finmarchicus (Copepoda: Crustacea) Exposed to Dispersed Oil. J Toxicol Environ Heal Part A 72:131 139. https://doi.org/10.1080/15287390802537313
Hansen BH, Tarrant AM, Salaberria I et al. (2017) Maternal polycyclic aromatic hydrocarbon (PAH) transfer and effects on offspring of copepods exposed to dispersed oil with and without oil droplets. J Toxicol Environ Heal Part A 80:881 894. https://doi.org/10.1080/15287394.2017.1352190
Hansen BH, Altin D, Rørvik SF et al. (2011) Comparative study on acute effects of water accommodated fractions of an artificially weathered crude oil on Calanus finmarchicus and Calanus glacialis (Crustacea: Copepoda). Sci Total Environ 409:704 709. https://doi.org/10.1016/j.scitotenv.2010.10.035
Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis, 3rd edn. Wiley-VCH
Hill V, Cota G (2005) Spatial patterns of primary production on the shelf, slope and basin of the Western Arctic in 2002. Deep Sea Res Part II 52:3344 3354. https://doi.org/10.1016/j.dsr2.2005.10.001
Hjorth M, Nielsen TG (2011) Oil exposure in a warmer Arctic: Potential impacts on key zooplankton species. Mar Biol 158:1339 1347. https://doi.org/10.1007/s00227-011-1653-3
Hsiao SIC (1978) Effects of crude oils on the growth of arctic marine phytoplankton. Environ Pollut 17:93 107. https://doi.org/10.1016/0013-9327(78)90043-5
Hsiao SIC, Kittlet DW, Foy MG (1978) Effects of crude oils and the oil dispersant corexit on primary production of arctic marine phytoplankton and seaweed. Environ Pollut 15:209 221
IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA
Jensen LK, Carroll J (2010) Experimental studies of reproduction and feeding for two Arctic-dwelling Calanus species exposed to crude oil. Aquat Biol 10:261 271. https://doi.org/10.3354/ab00286
Jespersen AM, Christoffersen K (1987) Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109:445 454
Karydis M (1981) The toxicity of crude oil for the marine alga Skeletonema costatum (Greville) Cleve in relation to nutrient limitation. Hydrobiologia 85:137 143. https://doi.org/10.1007/BF00006623
Kiørboe T, Møhlenberg F, Nicolajsen H (1982) Ingestion rate and gut clearance in the planktonic copepod Centropages hamatus (Lilljeborg) in relation to food concentration and temperature. Ophelia 21:181 194
Lacaze JC, Villedon de Naïde O (1976) Influence of illumination on phytotoxicity of crude oil. Mar Pollut Bull 7:73 76. https://doi.org/10.1016/0025-326X(76)90018-7
Lee RF (2003) Photo-oxidation and Photo-toxicity of Crude and Refined Oils. Spill Sci Technol Bull 8:157 162. https://doi.org/10.1016/S1353-2561(03)00015-X
Lewis M, Pryor R (2013) Toxicities of oils, dispersants and dispersed oils to algae and aquatic plants: Review and database value to resource sustainability. Environ Pollut 180:345 367. https://doi.org/10.1016/j.envpol.2013.05.001
Miljeteig C, Olsen AJ, Nordtug T et al. (2013) Sublethal exposure to crude oil enhances positive phototaxis in the calanoid copepod Calanus finmarchicus. Environ Sci Technol 47:14426 14433. https://doi.org/10.1021/es4037447
Møller EF, Maar M, Jónasdóttir SH et al. (2012) The effect of changes in temperature and food on the development of Calanus finmarchicus and Calanus helgolandicus populations. Limnol Oceanogr 57:211 220. https://doi.org/10.4319/lo.2012.57.1.0211
Møller EF, Nielsen TG, Richardson K (2006) The zooplankton community in the Greenland Sea: Composition and role in carbon turnover. Deep Res Part I Oceanogr Res Pap 53:76 93. https://doi.org/10.1016/j.dsr.2005.09.007
Nahrgang J, Dubourg P, Frantzen M et al. (2016) Early life stages of an arctic keystone species (Boreogadus saida) show high sensitivity to a water-soluble fraction of crude oil. Environ Pollut 218: https://doi.org/10.1016/j.envpol.2016.07.044
Nordtug T, Olsen AJ, Salaberria I et al. (2015) Oil droplet ingestion and oil fouling in the copepod Calanus finmarchicus exposed to mechanically and chemically dispersed crude oil. Environ Toxicol Chem 34:1899 1906. https://doi.org/10.1002/etc.3007
Nørregaard RD, Nielsen TG, Møller EF et al. (2014) Evaluating pyrene toxicity on Arctic key copepod species Calanus hyperboreus. Ecotoxicology 23:163 174. https://doi.org/10.1007/s10646-013-1160-z
Olsen AJ, Nordtug T, Altin D et al. (2013) Effects of dispersed oil on reproduction in the cold water copepod Calanus finmarchicus (Gunnerus). Environ Toxicol Chem 32:2045 55. https://doi.org/10.1002/etc.2273
Peck M (1992) Introduction to Linear Regression Analysis, 2nd edn. Wiley-Interscience, New York, USA
Pelletier MC, Burgess RM, Ho KT et al. (1997) Phototoxicity of individual polycyclic aromatic hydrocarbons and petroleum to marine invertebrate larvae and juveniles. Environ Toxicol Chem 16:2190 2199. https://doi.org/10.1002/etc.5620161029
R Core Team (2015) R: A language and environment for statistical computing
Rothrock DA, Yu Y, Maykut GA (1999) Thinning of the Arctic sea-ice cover. Geophys Res Lett 26:3469 3472. https://doi.org/10.1029/1999GL010863
Saco-Álvarez L, Bellas J, Nieto Ó et al. (2008) Toxicity and phototoxicity of water-accommodated fraction obtained from Prestige fuel oil and Marine fuel oil evaluated by marine bioassays. Sci Total Environ 394:275 282. https://doi.org/10.1016/j.scitotenv.2008.01.045
Santander-Avanceña SS, Sadaba RB, Taberna HS et al. (2016) Acute Toxicity of Water-Accommodated Fraction and Chemically Enhanced WAF of Bunker C Oil and Dispersant to a Microalga Tetraselmis tetrathele. Bull Environ Contam Toxicol 96:31 35. https://doi.org/10.1007/s00128-015-1696-0
Schwacke LH, Smith CR, Townsend FI et al. (2014) Health of Common Bottlenose Dolphins (Tursiops truncatus) in Barataria Bay, Louisiana, Following the Deepwater Horizon Oil Spill. Environ Sci Technol 48:93 103. https://doi.org/10.1021/es403610f
Shankar R, Shim WJ, An JG, Yim UH (2015) A practical review on photooxidation of crude oil: Laboratory lamp setup and factors affecting it. Water Res 68:304 315. https://doi.org/10.1016/J.WATRES.2014.10.012
Singer MM, Aurand D, Bragin GE et al. (2000) Standardization of the preparation and quantitation of water-accommodated fractions of petroleum for toxicity testing. Mar Pollut Bull 40:1007 1016. https://doi.org/10.1016/S0025-326X(00)00045-X
Steeman Nielsen E (1952) The use of radioactive carbon (CM) for measuring organic production in the sea. J Cons Cons Perm Inter Explor Mer 18:117 140
Thyrring J, Juhl BK, Holmstrup M et al. (2015) Does acute lead (Pb) contamination influence membrane fatty acid composition and freeze tolerance in intertidal blue mussels in arctic Greenland? Ecotoxicology 24:2036 2042. https://doi.org/10.1007/s10646-015-1539-0
Toxværd K, Pančić M, Eide HO et al. (2018) Effects of oil spill response technologies on the physiological performance of the Arctic copepod Calanus glacialis. Aquat Toxicol 199:65 76. https://doi.org/10.1016/J.AQUATOX.2018.03.032
Tremblay J-E, Gratton Y, Fauchot J, Price NM (2002) Climatic and oceanic forcing of new, net, and diatom production in the North Water. Deep Sea Res Part II 49:4927 4946. https://doi.org/10.1016/S0967-0645(02)00171-6
Tremblay J-É, Anderson LG, Matrai P et al. (2015) Global and regional drivers of nutrient supply, primary production and CO2 drawdown in the changing Arctic Ocean. Prog Oceanogr 139:171 196. https://doi.org/10.1016/j.pocean.2015.08.009
Vergeynst L, Wegeberg S, Aamand J et al. (2018) Biodegradation of marine oil spills in the Arctic with a Greenland perspective. Sci Total Environ 626:1243 1258. https://doi.org/10.1016/j.scitotenv.2018.01.173
Wolfe MF, Olsen HE, Gasuad KA et al. (1999) Induction of heat shock protein (hsp)60 in Isochrysis galbana exposed to sublethal preparations of dispersant and Prudhoe Bay crude oil. Mar Environ Res 47:473 489. https://doi.org/10.1016/S0141-1136(98)00132-9
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3 14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
The authors want to thank the crew of R/V Dana for help during field sampling. Sampling was carried out as part of the “North East Greenland Environmental Study Program” initiated by the Greenland Government. JT gratefully acknowledges financial support from the Independent Research Fund Denmark (Danmarks Frie Forskningsfond) during the writing of this paper (Individual Post-doctoral Grant no. 7027-00060B). J.M.H was supported by European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 752325.
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Lemcke, S., Holding, J., Møller, E.F. et al. Acute oil exposure reduces physiological process rates in Arctic phyto- and zooplankton. Ecotoxicology 28, 26–36 (2019). https://doi.org/10.1007/s10646-018-1995-4
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DOI: https://doi.org/10.1007/s10646-018-1995-4