Evaluating pyrene toxicity on Arctic key copepod species Calanus hyperboreus

Abstract

Calanus hyperboreus is a key species in the Arctic regions because of its abundance and role in the Arctic food web. Exploitation of the off shore oil reserves along Western Greenland is expected in the near future, and it is important to evaluate the acute and chronic effects of oil emissions to the ecosystem. In this study C. hyperboreus females were exposed to concentrations of 0, 0.1, 1, 10 and 100 nM pyrene and saturated concentrations measured to ~300 nM. Daily quantification of egg and faecal pellet production showed significant decreases in the pellet production, while the egg production was unaffected. The hatching success was also unaffected, although the total reproductive output was reduced with increased pyrene concentrations. Accumulation of pyrene in the copepods was higher in feeding than starving females and only trace amounts of the phase I metabolite 1-hydroxypyrene, were found. Lowered reproductive output, reduced grazing, and reduced ability to metabolize pyrene suggest that oil contamination may constitute a risk to C. hyperboreus recruitment, energy transfer in the food web and transfer of pyrene to higher trophic levels.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. AMAP (2007) Arctic oil and gas 2007. In: Arctic monitoring and assessment programme, Oslo

  2. Auel H, Hagen W (2002) Mesozooplankton community structure, abundance and biomass in the central Arctic Ocean. Mar Biol 140:1013–1021

    Article  Google Scholar 

  3. Barata C, Calbet A, Saiz E, Ortiz L, Bayona JM (2005) Predicting single and mixture toxicity of petrogenic polycyclic aromatic hydrocarbons to the copepod Oithona davisae. Environ Toxicol Chem 24:2992–2999

    CAS  Article  Google Scholar 

  4. Berrojalbiz N, Lacorte S, Calbet A, Saiz E, Barata C, Dachs J (2009) Accumulation and cycling of polycyclic aromatic hydrocarbons in zooplankton. Environ Sci Technol 43:2295–2301

    CAS  Article  Google Scholar 

  5. Cowles TJ, Remillard JF (1983) Effects of exposure to sublethal concentrations of crude oil on the copepod Centropages hamatus. Mar Biol 78:45–51

    CAS  Article  Google Scholar 

  6. Diercks AR, Highsmith RC, Asper VL, Joung D, Zhou Z, Guo L, Shiller AM, Joye SB, Teske AP, Norman G, Wade TL, Lohrenz SE (2010) Characterization of subsurface polycyclic aromatic hydrocarbons at the deepwater horizon site. Geophys Res Lett 37(20):L20602

    Google Scholar 

  7. Dutz J, Koski M, Jónasdóttir SH (2008) Copepod reproduction is unaffected by diatom aldehydes or lipid composition. Limnol Oceanogr 53:225–235

    CAS  Article  Google Scholar 

  8. Falk-Petersen S, Timofeev S, Pavlov V, Sargent JR (2006) Climate variability and possible effects on arctic food chains: the role of Calanus. In: Ørbaek JB et al (eds) Arctic alpine ecosystems and people in a changing environment. Springer, Berlin

    Google Scholar 

  9. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18–39

    Article  Google Scholar 

  10. Gouliarmou V, Smith KEC, de Jonge LW, Mayer P (2012) Measuring binding and speciation of hydrophobic organic chemicals at controlled freely dissolved concentrations and without phase separation. Anal Chem 84:1601–1608

    CAS  Article  Google Scholar 

  11. Grenvald JC, Nielsen TG, Hjorth M (2012) Effects of pyrene exposure and temperature on early development of two co-existing Arctic copepods. Ecotoxicology 22:184–198

    Article  Google Scholar 

  12. Henriksen MV, Madsen SJ, Nielsen TG, Møller EF, Henriksen KV, Markager S, Hansen BW (2012) Effects of temperature and food availability on feeding and egg production of Calanus hyperboreus from Disko Bay, western Greenland. Mar Ecol Prog Ser 447:109–126

    Article  Google Scholar 

  13. Hirche HJ (1991) Distribution of dominant calanoid copepod species in the Greenland Sea during late fall. Polar Biol 11:351–362

    Article  Google Scholar 

  14. Hirche HJ (2013) Long-term experiments on life span, reproductive activity and timing of reproduction in the Arctic copepod Calanus hyperboreus. Mar Biol. doi:10.1007/s00227-013-2242-4

    Google Scholar 

  15. Hirche HJ, Niehoff B (1996) Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea-field and laboratory observations. Polar Biol 16:209–219

    Article  Google Scholar 

  16. Hjorth M, Nielsen TG (2011) Oil exposure in a warmer Arctic: potential impacts on key zooplankton species. Mar Biol 158:1339–1347

    Article  Google Scholar 

  17. Hopcroft RR, Clarke C, Nelson RJ, Raskoff KA (2005) Zooplankton communities of the Arctic’s Canada Basin: the contribution by smaller taxa. Polar Biol 28:198–206

    Article  Google Scholar 

  18. Hydrocarbonstrategy (2009) Exploration and exploitation of hydrocarbons in Greenland. Bureau of minerals and petroleum, the Greenland home rule government, Nuuk

    Google Scholar 

  19. Hylland K (2006) Polycyclic aromatic hydrocarbon (PAH) ecotoxicology in marine ecosystems. J Toxicol Environ Health Part A 69:109–123

    CAS  Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. Jensen MH, Nielsen TG, Dahllöf I (2008) Effects of pyrene on grazing and reproduction of Calanus finmarchicus and Calanus glacialis from Disko Bay, West Greenland. Aquat Toxicol 87:99–107

    CAS  Article  Google Scholar 

  22. Jung-Madsen S, Nielsen TG, Grønkjær P, Hansen BW, Møller EF (2013) Early development of Calanus hyperboreus nauplii—Response to a changing ocean. Limnol Oceanog 58:2109–2121

    Google Scholar 

  23. Juul-Pedersen T, Nielsen TG, Michel C, Møller EF, Tiselius P, Thor P, Olesen M, Selander E, Gooding S (2006) Sedimentation following the spring bloom in Disko Bay, West Greenland, with special emphasis on the role of copepods. Mar Ecol Prog Ser 314:239–255

    Article  Google Scholar 

  24. Kjellerup S, Dünweber M, Swalethrop R, Nielsen TG, Møller EF, Markager S, Hansen BW (2012) Effects of a future warmer ocean on the coexisting copepods Calanus finmarchicus and C. glacialis in Disko Bay, western Greenland. Mar Ecol Prog Ser 447:87–108

    CAS  Article  Google Scholar 

  25. Law RJ, Kelly C, Baker K, Jones J, McIntosh AD, Moffat CF (2002) Toxic equivalency factors for PAH and their applicability in shellfish pollution monitoring studies. J Environ Monit 4:383–388

    CAS  Article  Google Scholar 

  26. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306

    CAS  Article  Google Scholar 

  27. Lotufo GR (1997) Toxicity of sediment-associated PAHs to an estuarine copepod: effects on survival, feeding, reproduction and behavior. Mar Environ Res 44:149–166

    CAS  Article  Google Scholar 

  28. Lotufo GR (1998) Lethal and sublethal toxicity of sediment-associated fluoranthene to benthic copepods: application of the critical-body-residue approach. Aquat Toxicol 44:17–30

    CAS  Article  Google Scholar 

  29. Madsen SD, Nielsen TG, Hansen BW (2001) Annual population development and production by Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, western Greenland. Mar Biol 139:75–93

    Article  Google Scholar 

  30. Madsen S, Nielsen TG, Tervo OM, Söderkvist J (2008) Importance of feeding for egg production in Calanus finmarchicus and C. glacialis during the Arctic spring. Mar Ecol Prog Ser 353:177–190

    CAS  Article  Google Scholar 

  31. May WE, Wasik SP (1978) Determination of the solubility behavior of some polycyclic aromatic hydrocarbons in water. Anal Chem 50:997–1000

    CAS  Article  Google Scholar 

  32. Niehoff B (1998) The gonad morphology and maturation in Arctic Calanus species. J Mar Syst 15:53–59

    Article  Google Scholar 

  33. Niehoff B (2007) Life history strategies in zooplankton communities: the significance of female gonad morphology and maturation types for the reproductive biology of marine calanoid copepods. Prog Oceanogr 74:1–47

    Article  Google Scholar 

  34. Nielsen TG, Hansen BW (1995) Plankton community structure and carbon cycling on the western coast of Greenland during and after the sedimentation of a diatom bloom. Mar Ecol Prog Ser 125:239–257

    CAS  Article  Google Scholar 

  35. Oil in the Sea III (2003) Oil in the sea III: inputs, fates and effects. The National Academies Press, Washington

    Google Scholar 

  36. Pelletier MC, Burgess RM, Ho KT, Kuhn A, McKinney RA, Rybe SA (1997) Phototoxicity of individual polycyclic aromatic hydrocarbons and petroleum to marine invertebrate larvae and juveniles. Environ Toxicol Chem 16:2190–2199

    CAS  Article  Google Scholar 

  37. Plourde S, Joly P, Runge JA, Dodson J, Zakardjian B (2003) Life cycle of Calanus hyperboreus in the lower St. Lawrence Estuary and its relationship to local environmental conditions. Mar Ecol Prog Ser 255:219–233

    Article  Google Scholar 

  38. Reigstad M, Riser C, Svenson C (2005) Fate of copepod faecal pellets and the role of Oithona spp. Mar Ecol Prog Ser 304:265-270

    Google Scholar 

  39. Rewitz KF, Styrishave B, Lobner-Olesen A, Andersen O (2006) Marine invertebrate cytochrome P450: emerging insights from vertebrate and insect analogies. Comp Biochem Physiol Part C 143:363–381

    Google Scholar 

  40. Scott CL, Kwasniewski S, Falk-Petersen S, Sargent JR (2000) Lipids and life strategies of Calanus finmarchicus, Calanus glacialis and Calanus hyperboreus in late autumn, Kongsfjorden, Svalbard. Polar Biol 23:510–516

    Article  Google Scholar 

  41. Socio-economic aspects (2004) Report on socio-economic aspects of hydrocarbon and exploitation and exploration in Greenland. Bureau of Minerals and Petroleum, the Greenland Home Rule Government, Nuuk

    Google Scholar 

  42. Statistics Greenland (2012) Grønlands Udenrigshandel 2011, vol 1. Udenrigshandel, Nuuk, p 1–19

  43. Swalethorp R, Kjellerup S, Dünweber M, Nielsen TG, Møller EF, Rysgaard S, Hansen BW (2011) Grazing, egg production, and biochemical evidence of differences in the life strategies of Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, western Greenland. Mar Ecol Prog Ser 429:125–144

    Article  Google Scholar 

  44. Tairova ZM, Giessing AMB, Hansen R, Andersen O (2009) 1-Hydroxypyrene as a biomarker of PAH exposure in the marine polychaete Nereis diversicolor. Mar Environ Res 67:38–46

    CAS  Article  Google Scholar 

  45. Tairova ZM, Strand J, Chevalier J, Andersen O (2012) PAH biomarkers in common eelpout (Zoarces viviparus) from Danish waters. Mar Environ Res 75:45–53

    CAS  Article  Google Scholar 

  46. Thor P, Nielsen TG, Juul-Pedersen T, Michel C, Møller EF, Dahl K, Selander E, Gooding S (2005) Post-spring bloom community structure of pelagic copepods in the Disko Bay, Western Greenland. J Plankton Res 27:341–356

    CAS  Article  Google Scholar 

  47. Varanasi U (1989) Metabolism of polycyclic hydrocarbons in the aquatic environments. CRC Press, Boca Ranton, FL

  48. van Wezel AP, Opperhuizen A (1995) Narcosis due to environmental pollutants in aquatic organisms: residue-based toxicity, mechanisms, and membrane burdens. Crit Rev Toxicol 25:255–279

    Article  Google Scholar 

  49. Welch HE, Bergmann MA, Siferd TD, Martin KA, Curtis MF, Crawford RE, Conover RJ, Hob H (1992) Energy flow through the marine ecosystem of the Lancaster Sound region, arctic Canada. Arctic 45:343–357

    Google Scholar 

Download references

Acknowledgments

This study was funded by the Carlsberg Foundation, Greenland Climate Research Center (GCRC Grant 6505), Bureau of Minerals and Petroleum, Greenland, Selskabet for Arktisk Forskning og Teknologi, Knud Højgårds Fond and the Oticon Foundation. The fieldwork took place at Arctic Station (University of Copenhagen, Qerqertarsuaq)—a big thanks to the station manager Ole Stecher and staff and to the crew of RV Porsild for providing a great working environment. We would especially like to thank Abel Brandt and Johannes Mølgaard, who with their hard work, good spirits and limitless knowledge on local conditions made our work on the sea ice possible.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Torkel Gissel Nielsen.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nørregaard, R.D., Nielsen, T.G., Møller, E.F. et al. Evaluating pyrene toxicity on Arctic key copepod species Calanus hyperboreus . Ecotoxicology 23, 163–174 (2014). https://doi.org/10.1007/s10646-013-1160-z

Download citation

Keywords

  • Calanus hyperboreus
  • PAH
  • Pyrene
  • Faecal pellet production
  • Egg production