New insights into the seasonal diet of Antarctic krill using triacylglycerol and phospholipid fatty acids, and sterol composition

  • Jessica A. EricsonEmail author
  • Nicole Hellessey
  • Peter D. Nichols
  • Stephen Nicol
  • So Kawaguchi
  • Nils Hoem
  • Patti Virtue
Original Paper


Fatty acid analysis for estimating dietary sources in marine predators is a powerful tool in food web research. However, questions have been raised about using fatty acids as dietary indicators from whole lipid samples, rather than from separate lipid classes. A drawback of scientific field-based studies is that samples are rarely collected over extended periods, precluding seasonal dietary comparisons. We used fisheries samples obtained over one year to investigate seasonal variations in the fatty acid composition of separated phospholipids and triacylglycerols of Antarctic krill (Euphausia superba). Seasonal variation was observed in fatty acid biomarkers within triacylglycerol and phospholipid fractions of krill. Fatty acids in krill triacylglycerols (thought to best represent recent diet), reflected omnivorous feeding with highest percentages of flagellate biomarkers (18:4n-3) in summer, and diatom biomarkers (16:1n-7c) in autumn, winter and spring. Carnivory biomarkers (∑ 20:1 + 22:1 and 18:1n-9c/18:1n-7c) in krill were higher in autumn. Phospholipid fatty acids were less variable and higher in 20:5n-3 and 22:6n-3, which are essential components of cell membranes. Sterol composition did not yield detailed dietary information, but percentages and quantities of cholesterol, the major krill sterol, were significantly higher in winter and spring compared with summer and autumn. Copepod markers ∑ 20:1 + 22:1 were not strongly associated with the triacylglycerol fraction during some seasons, and neither was 18:4n-3. Krill might mobilise 18:4n-3 from triacylglycerols to phospholipids for conversion to long-chain (≥ C20) polyunsaturated fatty acids, which would have implications for its role as a dietary biomarker. For the first time, we demonstrate the dynamic seasonal relationship between specific biomarkers and krill lipid classes.


Antarctic krill Fatty acid biomarkers Inferred diet Phospholipids Sterols Triacylglycerols 



We would like to extend our warmest gratitude to the Captain and crew of Aker Biomarine’s FV Saga Sea for collecting, carefully packaging and storing the krill used for this study, so as to maintain premium sample integrity. We also thank Dr Andy Revill for facilitating this research, and Mina Brock for technical assistance in the laboratory. This research was funded by Australian Research Council Linkage Grant LP140100412 between the Australian Antarctic Division, Commonwealth Scientific and Industrial Research Organization, Institute for Marine and Antarctic Studies (University of Tasmania), Griffith University and Aker Biomarine.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no competing interest.

Supplementary material

300_2019_2573_MOESM1_ESM.docx (25 kb)
Supplementary file1 (DOCX 26 kb)


  1. Alonzo F, Nicol S, Virtue P, Nichols PD (2003) Lipids as trophic markers in Antarctic krill, I. Validation under controlled laboratory conditions. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys Publishers, Leiden, pp 121–128Google Scholar
  2. Alonzo F, Virtue P, Nicol S, Nichols PD (2005a) Lipids as trophic markers in Antarctic krill. II. Lipid composition of the body and digestive gland of Euphausia superba in controlled conditions. Mar Ecol Prog Ser 296:65–79CrossRefGoogle Scholar
  3. Alonzo F, Virtue P, Nicol S, Nichols PD (2005b) Lipids as trophic markers in Antarctic krill. III. Temporal changes in digestive gland lipid composition of Euphausia superba in controlled conditions. Mar Ecol Prog Ser 296:81–91CrossRefGoogle Scholar
  4. Atkinson A, Meyer B, Stübing D, Hagen W, Schmidt K, Bathmann UV (2002) Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter – II. Juveniles and adults. Limnol Oceanogr 47:953–966CrossRefGoogle Scholar
  5. Auerswald L, Meyer B, Teschke M, Hagen W, Kawaguchi S (2015) Physiological response of adult Antarctic krill, Euphausia superba, to long-term starvation. Polar Biol 38:763–780CrossRefGoogle Scholar
  6. Barrett S, Volkman J, Dunstan G (1995) Sterols in 14 species of marine diatoms (Bacillariophyta). J Phycol 31:360–369CrossRefGoogle Scholar
  7. Bell M, Dick J, Anderson T, Pond D (2007) Application of liposome and stable isotope tracer techniques to study polyunsaturated fatty acid biosynthesis in marine zooplankton. J Plankton Res 29:417–422CrossRefGoogle Scholar
  8. Bligh EG, Dyer W (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefGoogle Scholar
  9. Bottino NR (1974) The fatty acids of Antarctic phytoplankton and euphausiids. Fatty acid exchange among trophic levels of the Ross Sea. Mar Biol 27:197–204CrossRefGoogle Scholar
  10. Clarke A (1980) The biochemical composition of krill, Euphausia superba Dana, from South Georgia. J Exp Mar Bio Ecol 43:221–236CrossRefGoogle Scholar
  11. Clarke A (1984) Lipid content and composition of Antarctic krill, Euphausia superba Dana. J Crustac Biol 4:285–294CrossRefGoogle Scholar
  12. Dalsgaard J, St John M, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefGoogle Scholar
  13. Ericson JA, Hellessey N, Nichols PD, Kawaguchi S, Nicol S, Hoem N, Virtue P (2018) Seasonal and interannual variations in the fatty acid composition of adult Euphausia superba Dana, 1850 (Euphausiacea) samples derived from the Scotia Sea krill fishery. J Crustac Biol. Google Scholar
  14. Falk-Petersen S, Hagen W, Kattner G, Clarke A, Sargent J (2000) Lipids, trophic relationships, and biodiversity in Arctic and Antarctic krill. Can J Fish Aquat Sci 57:178–191CrossRefGoogle Scholar
  15. Fricke H, Gercken G, Schreiber W, Oehlenschlager J (1984) Lipid, sterol and fatty acid composition of Antarctic krill (Euphausia superba Dana). Lipids 19:821–827CrossRefGoogle Scholar
  16. Gigliotti JC, Davenport MP, Beamer SK, Tou JC, Jaczynski J (2011) Extraction and characterisation of lipids from Antarctic krill (Euphausia superba). Food Chem 125:1028–1036CrossRefGoogle Scholar
  17. Graeve M, Hagen W, Kattner G (1994) Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods. Deep Sea Res Part I Oceanogr Res Pap 41:915–924CrossRefGoogle Scholar
  18. Hagen W, Kattner G, Graeve M (1993) Calanoides acutus and Calanus propinquus, Antarctic copepods with different lipid storage modes via wax esters or triacylglycerols. Mar Ecol Prog Ser 97:135–142CrossRefGoogle Scholar
  19. Hagen W, Kattner G, Terbruggen A, Van Vleet ES (2001) Lipid metabolism of the Antarctic krill Euphausia superba and its ecological implications. Mar Biol 139:95–104CrossRefGoogle Scholar
  20. Hellessey N, Ericson JA, Nichols PD, Kawaguchi S, Nicol S, Hoem N, Virtue P (2018) Seasonal and interannual variation in the lipid content and composition of Euphausia superba Dana 1850 (Euphausiacea) samples derived from the Scotia Sea fishery. J Crustac Biol. Google Scholar
  21. Ju S-J, Harvey HR (2004) Lipids as markers of nutritional condition and diet in the Antarctic krill Euphausia superba and Euphausia crystallorophias during austral winter. Deep Sea Res Part II Top Stud Oceanogr 51:2199–2214CrossRefGoogle Scholar
  22. Kanazawa A (2001) Sterols in marine invertebrates. Fish Sci 67:997–1007CrossRefGoogle Scholar
  23. Kattner G, Hagen W (1995) Polar herbivorous copepods – different pathways in lipid biosynthesis. ICES J Mar Sci 52:329–335CrossRefGoogle Scholar
  24. Kattner G, Hagen W (1998) Lipid metabolism of the Antarctic euphausiid Euphausia crystallorophias and its ecological implications. Mar Ecol Prog Ser 170:203–213CrossRefGoogle Scholar
  25. Kattner G, Hagen W, Lee RF, Campbell R, Deibel D, Falk-Petersen S, Graeve M, Hansen BW, Hirche HJ, Jónasdóttir SH, Madsen ML, Mayzaud P, Müller-Navarra D, Nichols PD, Paffenhöfer GA, Pond D, Saito H, Stübing D, Virtue P (2007) Perspectives on marine zooplankton lipids. Can J Fish Aquat Sci 64:1628–1639CrossRefGoogle Scholar
  26. Martin-Creuzburg D, von Elert E (2009) Ecological significance of sterols in aquatic food webs. In: Arts MT, Brett MT, Kainz M (eds) Lipids in Aquatic Ecosystems. Springer, New york, pp 43–64CrossRefGoogle Scholar
  27. Mayzaud P (1997) Spatial and life-cycle changes in lipid and fatty acid structure of the Antarctic euphausiid Euphausia superba. In: Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 284–294Google Scholar
  28. Mayzaud P, Albessard E, Cuzin-Roudy J (1998) Changes in lipid compostion of the Antarctic krill Euphausia superba in the Indian sector of the Antarctic ocean: influence of geographical location, sexual maturity stage and distribution among organs. Mar Ecol Prog Ser 173:149–162CrossRefGoogle Scholar
  29. Mayzaud P, Virtue P, Albessard E (1999) Seasonal variations in the lipid and fatty acid composition of the euphausiid Meganyctiphanes norvegica from the Ligurian Sea. Mar Ecol Prog Ser 186:199–210CrossRefGoogle Scholar
  30. Mayzaud P, Albessard E, Virtue P, Boutoute M (2000) Environmental constraints on the lipid composition and metabolism of euphausiids: the case of Euphausia superba and Meganyctiphanes norvegica. Can J Fish Aquat Sci 57:91–103CrossRefGoogle Scholar
  31. Monroig O, Tocher D, Navarro J (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs 11:3998–4018CrossRefGoogle Scholar
  32. Murphy EJ, Morris DJ, Watkins JL, Priddle J (1988) Scales of interaction between Antarctic krill and the environment. In: Sahrhage D (ed) Antarctic Ocean and Resources Variability. Springer, Berlin.Google Scholar
  33. Murphy EJ, Watkins JL, Trathan PN, Reid K, Meredith MP, Thorpe SE, Johnston NM, Clarke A, Tarling GA, Collins MA, Forcada J, Shreeve RS, Atkinson A, Korb R, Whitehouse MJ, Ward P, Rodhouse PG, Enderlein P, Hirst AG, Martin AR, Hill SL, Staniland IJ, Pond DW, Briggs DR, Cunningham NJ, Fleming AH (2007) Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web. Philos Trans R Soc B 362:113–148CrossRefGoogle Scholar
  34. Nichols PD, Skerratt JH, Davidson A, Burton H, McMeekin TA (1991) Lipids of cultured Phaeocystis pouchetii: signatures for food-web, biogeochemical and environmental studies in Antarctica and the Southern ocean. Phytochemistry 30:3209–3214CrossRefGoogle Scholar
  35. Nicol S, Foster J, Kawaguchi S (2011) The fishery for Antarctic krill – recent developments. Fish Fish 13:30–40CrossRefGoogle Scholar
  36. O’Brien C, Virtue P, Kawaguchi S, Nichols PD (2011) Aspects of krill growth and condition during late winter-early spring off East Antarctica (110–130°E). Deep Sea Res Part II Top Stud Oceanogr 58:1211–1221CrossRefGoogle Scholar
  37. Parrish C, Abrajano T, Budge S, Helleur R, Hudson E, Pulchan K, Ramos C (2000) Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. The Handbook of Environmental Chemistry, vol 5. Part D Marine Chemistry. Springer, Berlin, pp 193–223Google Scholar
  38. Phleger CF, Nelson MM, Mooney BD, Nichols PD (2002) Interannual and between species comparison of the lipids, fatty acids and sterols of Antarctic krill from the US AMLR Elephant Island survey area. Comp Biochem Physiol Part B 131:733–747CrossRefGoogle Scholar
  39. Reiss CS, Walsh J, Goebel ME (2015) Winter preconditioning determines feeding ecology of Euphausia superba in the Antarctic Peninsula. Mar Ecol Prog Ser 519:89–101CrossRefGoogle Scholar
  40. Schmidt K, Atkinson A (2016) Feeding and food processing in Antarctic krill (Euphausia superba Dana). In: Siegel V (ed) Biology and Ecology of Antarctic Krill. Springer, Cham, pp 175–224CrossRefGoogle Scholar
  41. Schmidt K, Atkinson A, Petzke K, Voss M, Pond D (2006) Protozoans as a food source for Antarctic krill, Euphausia superba: complementary insights from stomach content, fatty acids, and stable isotopes. Limnol Oceanogr 51:2409–2427CrossRefGoogle Scholar
  42. Schmidt K, Atkinson A, Pond DW, Ireland LC (2014) Feeding and overwintering of Antarctic krill across its major habitats: the role of sea ice cover, water depth, and phytoplankton abundance. Limnol Oceanogr 59:17–36CrossRefGoogle Scholar
  43. Stübing D, Hagen W (2003) Fatty acid biomarker ratios – suitable trophic indicators in Antarctic euphausiids? Polar Biol 26:774–782CrossRefGoogle Scholar
  44. Stübing D, Hagen W, Schmidt K (2003) On the use of lipid biomarkers in marine food web analyses: an experimental case study on the Antarctic krill, Euphausia superba. Limnol Oceanogr 48:1685–1700CrossRefGoogle Scholar
  45. Trathan PN, Hill SL (2016) The importance of krill predation in the Southern Ocean. In: Siegel V (ed) Biology and Ecology of Antarctic Krill. Springer, Switzerland, pp 321–350CrossRefGoogle Scholar
  46. Virtue P, Nichols PD, Nicol S, McMinn A, Sikes EL (1993a) The lipid composition of Euphausia superba Dana in relation to the nutritional value of Phaeocystis pouchetii (Hariot) Lagerheim. Antarct Sci 5:169–177CrossRefGoogle Scholar
  47. Virtue P, Nicol S, Nichols PD (1993b) Changes in the digestive gland of Euphausia superba during short-term starvation – lipid class, fatty acid and sterol content and composition. Mar Biol 117:441–448Google Scholar
  48. Virtue P, Nichols PD, Nicol S, Hosie G (1996) Reproductive trade-off in male Antarctic krill, Euphausia superba. Mar Biol 126:521–527CrossRefGoogle Scholar
  49. Virtue P, Mayzaud P, Albessard E, Nichols PD (2000) Use of fatty acids as dietary indicators in northern krill, Meganyctiphanes norvegica, from northeastern Atlantic, Kattegat, and Mediterranean waters. Can J Fish Aquat Sci 57:104–114CrossRefGoogle Scholar
  50. Virtue P, Meyer B, Freier U, Nichols PD, Jia Z, King R, Virtue J, Swadling KM, Meiners KM, Kawaguchi S (2016) Condition of larval (furcilia VI) and one year old juvenile Euphausia superba during the winter–spring transition in East Antarctica. Deep Sea Res Part II Top Stud Oceanogr 131:182–188CrossRefGoogle Scholar

Copyright information

© Crown 2019

Authors and Affiliations

  1. 1.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  2. 2.Antarctic Climate & Ecosystems Cooperative Research CentreHobartAustralia
  3. 3.CSIRO Oceans and AtmosphereHobartAustralia
  4. 4.Cawthron InstituteNelsonNew Zealand
  5. 5.Australian Antarctic DivisionKingstonAustralia
  6. 6.Aker BiomarineLysakerNorway

Personalised recommendations