Advertisement

Ecotoxicology

, Volume 28, Issue 1, pp 26–36 | Cite as

Acute oil exposure reduces physiological process rates in Arctic phyto- and zooplankton

  • Signe LemckeEmail author
  • Johnna Holding
  • Eva Friis Møller
  • Jakob Thyrring
  • Kim Gustavson
  • Thomas Juul-Pedersen
  • Mikael K. Sejr
Article

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.

Keywords

Arctic WAF Oil spill Calanus finmarchicus Phytoplankton Phototoxicity 

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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, CopenhagenGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis, 3rd edn. Wiley-VCHGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 221CrossRefGoogle Scholar
  25. 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, USAGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. Jespersen AM, Christoffersen K (1987) Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109:445 454Google Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 194CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. Peck M (1992) Introduction to Linear Regression Analysis, 2nd edn. Wiley-Interscience, New York, USAGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. R Core Team (2015) R: A language and environment for statistical computingGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 140CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Signe Lemcke
    • 1
    Email author
  • Johnna Holding
    • 1
  • Eva Friis Møller
    • 1
    • 2
  • Jakob Thyrring
    • 3
    • 4
  • Kim Gustavson
    • 5
  • Thomas Juul-Pedersen
    • 6
  • Mikael K. Sejr
    • 1
    • 7
  1. 1.Department of Bioscience, Arctic Research CentreAarhus UniversityAarhus CDenmark
  2. 2.Department of Bioscience, Marine Diversity and Experimental EcologyAarhus UniversityRoskildeDenmark
  3. 3.Department of ZoologyUniversity of British ColumbiaVancouver British ColumbiaCanada
  4. 4.British Antarctic SurveyCambridgeUnited Kingdom
  5. 5.Department of Bioscience, Arctic EnvironmentAarhus UniversityRoskildeDenmark
  6. 6.Greenland Institute of Natural ResourcesGreenland Climate Research CentreNuukGreenland
  7. 7.Department of Bioscience, Marine EcologyAarhus UniversitySilkeborgDenmark

Personalised recommendations