Advertisement

Marine Biology

, Volume 156, Issue 7, pp 1459–1473 | Cite as

Comparative lipid dynamics of euphausiids from the Antarctic and Northeast Pacific Oceans

  • Se-Jong Ju
  • Hyung-Ku Kang
  • Woong Seo Kim
  • H. Rodger Harvey
Original Paper

Abstract

To better understand the feeding and reproductive ecology of euphausiids (krill) in different ocean environments, lipid classes and individual lipid components of four different species of euphausiids from Northeast Pacific (temperate species) and Southern Ocean (Antarctic species) were analyzed in animals from multiple life stages and seasons. The dominant krill species in the Northeast Pacific Euphausia pacifica and Thysanoessa spinifera, were compared to the two major Antarctic species, Euphausia superba and E. crystallorophias. Analysis comprised total lipid and lipid classes together with individual fatty acid and sterol composition in adults, juveniles, and larvae. Antarctic krill had much higher lipid content than their temperate relatives (10–50 and 5–20% of dry mass for Antarctic and temperate species, respectively) with significant seasonal variations observed. Phospholipids were the dominant lipid class in both temperate krill species, while neutral storage lipids (wax esters and triacylglycerols for E. crystallorophias and E. superba, respectively) were the major lipid class in Antarctic krill and accounted for up to 40% of the total lipid content. Important fatty acids, specifically 16:0, 18:1ω9, 20:5ω3, and 22:6ω3, were detected in all four krill species, with minor differences between species and seasons. Detailed lipid profiles suggest that krill alter their lipid composition with life stage and season. In particular, larval Antarctic krill appear to utilize alternate food resources (i.e., sea-ice associated organisms) during austral winter in contrast to juveniles and adults (i.e., seston and copepods). Lipid dynamics in krill among krill in both systems appear closely linked to their life cycle and environmental conditions including food availability, and can provide a more complete comparative ecology of euphausiids in these environmentally distinct systems.

Keywords

Lipid Class Fatty Alcohol Total Lipid Content Temperate Species Antarctic Krill 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank William Peterson, Tracy Shaw, Leah Feinberg, Rachael Dyda, Steve McGuire and Susan Klosterhaus for their assistance in the collection of euphausiids. This work was supported by the NSF through the Southern Ocean GLOBEC program (OPP-9910043 to HRH) and NOAA through the Northeast Pacific GLOBEC program (OCE-0000732 to HRH through NSF). S.-J. Ju was also partially supported by KORDI projects (PP00720 and PE9830V) and the industrial and academic outstanding researcher invitation program sponsored by KORP. This manuscript is contribution No. 4269 of The University of Maryland Center for Environmental Science and contribution No. 630 of USGLOBEC program.

References

  1. Alber CS, Kattner G, Hagen W (1996) The compositions of wax esters, triacylglycerols and phospholipids in Arctic and Antarctic copepods: evidence of energetic adaptations. Mar Chem 55:347–358. doi: https://doi.org/10.1016/S0304-4203(96)00059-X CrossRefGoogle Scholar
  2. Albessard EP, Mayzaud P (2003) Influence tropho-climatic environment and reproduction on lipid composition of the euphausiid Meganyctiphanes norvegica in the Ligurian Sea, the Clyde Sea and the Kattegat. Mar Ecol Prog Ser 253:217–232. doi: https://doi.org/10.3354/meps253217 CrossRefGoogle Scholar
  3. Albessard EP, Mayzaud P, Cuzin-Roudy J (2001) Variation of lipid classes among organs of the Northern krill, Meganyctiphanes norvegica, with respect to reproduction. Comp Biochem Physiol 129 A:373–390CrossRefGoogle Scholar
  4. Atkinson A, Snÿder R (1997) Krill-copepod interactions at South Georgia, Antarctica, I. Omnivory by Euphausia superba. Mar Ecol Prog Ser 160:63–76. doi: https://doi.org/10.3354/meps160063 CrossRefGoogle Scholar
  5. Atkinson A, Meyer B, Stübing D, Hagen W, Schmidt A, Bathmann UV (2002) Feeding and energy budgets of Antarctic Euphausia superba at the onset of winter—I. Juveniles and adults. Limnol Oceanogr 47(4):953–966CrossRefGoogle Scholar
  6. Barrett SM, Volkman JK, Dunstan GA, Leroi JM (1995) Sterols of 14 species of marine diatoms (bacillariophyta). J Phycol 31:360–369. doi: https://doi.org/10.1111/j.0022-3646.1995.00360.x CrossRefGoogle Scholar
  7. Bottino NR (1974) The fatty acids of Antarctic phytoplankton and euphausiids. Fatty acid exchange among trophic levels of the Ross Sea. Mar Biol (Berl) 27:197–204. doi: https://doi.org/10.1007/BF00391944 CrossRefGoogle Scholar
  8. Brinton E (1976) Population biology of Euphausia pacifica off southern California. Fish Bull (Wash D C) 74:733–762Google Scholar
  9. Clark A (1984) Lipid content and composition of Antarctic krill Euphausia superba Dana. J Crustac Biol 4:285–294CrossRefGoogle Scholar
  10. Cuzin-Roudy J, Buchholz F (1999) Ovarian development and spawning in relation to moult cycle in Northern krill, Meganyctiphanes norvegica (Crustacea: Euphausiacea), along a climatic gradient. Mar Biol (Berl) 133:236–249. doi: https://doi.org/10.1007/s002270050466 CrossRefGoogle Scholar
  11. Dalsgaard J, John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340. doi: https://doi.org/10.1016/S0065-2881(03)46005-7 CrossRefGoogle Scholar
  12. Destaillats F, Angers P (2002) One-step methodology for the synthesis of FA picolinyl esters from intact lipids. J Am Oil Chem Soc 79:253–256CrossRefGoogle Scholar
  13. Falk-Petersen S, Sargent JR, Lønne OJ, Timofeev S (1999) Functional biodiversity of lipids in Antarctic zooplankton: Calanoides acutus, Calanus propinquus, Thysanoessa macrura and Euphausia crystallorophias. Polar Biol 21:37–47. doi: https://doi.org/10.1007/s003000050330 CrossRefGoogle 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 57:178–191. doi: https://doi.org/10.1139/cjfas-57-S3-178 CrossRefGoogle Scholar
  15. Feinberg LR, Peterson WT (2003) Variability in duration and intensity of euphausiid spawning off central Oregon, 1996–2001. Prog Oceanogr 57:363–379. doi: https://doi.org/10.1016/S0079-6611(03)00106-X CrossRefGoogle Scholar
  16. Goad LJ (1981) Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl Chem 51:837–852. doi: https://doi.org/10.1351/pac198153040837 CrossRefGoogle Scholar
  17. Hagen W, Auel H (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton. Zoology 104:313–326. doi: https://doi.org/10.1078/0944-2006-00037 CrossRefGoogle Scholar
  18. Hagen W, Van Vleet ES, Kattner G (1996) Seasonal lipid storage as overwintering strategy of Antarctic krill. Mar Ecol Prog Ser 134:85–89. doi: https://doi.org/10.3354/meps134085 CrossRefGoogle 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 (Berl) 139(1):95–104. doi: https://doi.org/10.1007/s002270000527 CrossRefGoogle Scholar
  20. Harrington SA, Thomas PG (1987) Observations on spawning by Euphausia crystallorophias from waters adjacent to Enderby Land (East Antarctica) and speculations on the early ontogenetic ecology of neritic euphausiids. Polar Biol 7:93–95. doi: https://doi.org/10.1007/BF00570446 CrossRefGoogle Scholar
  21. Harvey HR, Eglinton G, O’Hara SCM, Corner EDS (1987) Biotransformation and assimilation of dietary lipids by Calanus feeding on a dinoflagellate. Geochim Cosmochim Acta 51:3030–3041. doi: https://doi.org/10.1016/0016-7037(87)90376-0 CrossRefGoogle Scholar
  22. Harvey HR, O’Hara SCM, Eglinton G, Corner EDS (1989) The comparative fate of dinosterol and cholesterol in copepod feeding: implications for a conservative molecular biomarker in the marine water column. Org Geochem 14(6):635–641. doi: https://doi.org/10.1016/0146-6380(89)90042-9 CrossRefGoogle Scholar
  23. Hazel JR (1985) Determination of the phospholipid composition of trout gill by Iatroscan TLC/FID: effect of thermal acclimation. Lipids 20:516–520. doi: https://doi.org/10.1007/BF02534892 CrossRefGoogle Scholar
  24. Huntley ME, Nordhausen W, Lopez MDG (1994) Elemental composition, metabolic activity and growth of Antarctic krill Euphausia superba during winter. Mar Ecol Prog Ser 107:23–40. doi: https://doi.org/10.3354/meps107023 CrossRefGoogle Scholar
  25. 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 51:2199–2214. doi: https://doi.org/10.1016/j.dsr2.2004.08.004 CrossRefGoogle Scholar
  26. Ju S-J, Kucklick JR, Kozlova T, Harvey HR (1997) Lipid accumulation and fatty acid composition during maturation of three pelagic fish species in Lake Baikal. J Great Lakes Res 23(3):241–253CrossRefGoogle Scholar
  27. Ju S-J, Harvey HR, Gómez-Gutiérrez J, Peterson WT (2006) The role of lipids during embryonic development of the euphausiids Euphausia pacifica and Thysanoessa spinifera. Limnol Oceanogr 51(5):2398–2408CrossRefGoogle Scholar
  28. Kattner G, Hagen W (1998) Lipid metabolism of the Antarctic euphausiid Euphausia crystallorophias and its ecological implication. Mar Ecol Prog Ser 170:203–213. doi: https://doi.org/10.3354/meps170203 CrossRefGoogle Scholar
  29. Lee RF, Nevenzel JC, Paffenhöfer G-A (1971) Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Mar Biol (Berl) 9:99–108. doi: https://doi.org/10.1007/BF00348249 CrossRefGoogle Scholar
  30. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306. doi: https://doi.org/10.3354/meps307273 CrossRefGoogle Scholar
  31. Littell RC, Millken GA, Stroup WW, Wolfinger RD (1999) SAS System for mixed models. SAS Institute Inc., CaryGoogle Scholar
  32. Longhurst AR (1985) The structure and evolution of plankton communities. Prog Oceanogr 15:1–35. doi: https://doi.org/10.1016/0079-6611(85)90036-9 CrossRefGoogle Scholar
  33. Mannino A, Harvey HR (1999) Lipid composition in particulate and dissolved organic matter in the Delaware Estuary: sources and diagenetic patterns. Geochim Cosmochim Acta 63:2219–2235. doi: https://doi.org/10.1016/S0016-7037(99)00128-3 CrossRefGoogle Scholar
  34. Marr JWS (1962) The natural history and geography of Antarctic krill (Euphauisa superba Dana). Discov Rep 32:33–464Google Scholar
  35. Mauchline J (1980) The biology of mysids and euphausiids. Adv Mar Biol 18:373–623. doi: https://doi.org/10.1016/S0065-2881(08)60372-7 CrossRefGoogle Scholar
  36. Mauchline J, Fisher LR (1969) The biology of euphausiids. Adv Mar Biol 7:1–454. doi: https://doi.org/10.1016/S0065-2881(08)60471-X CrossRefGoogle Scholar
  37. Mayzaud P, Boutoute M, Alonzo F (2003) Lipid composition of the euphausiids Euphausia vallentini and Thysanoessa macrura during summer in the southern Indian Ocean. Antarct Sci 15:463–475. doi: https://doi.org/10.1017/S0954102003001573 CrossRefGoogle Scholar
  38. Meyer B, Atkinson A, Stübing D, Oettl B, Hagen W, Bathmann UV (2002) Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter – I. Furcilia III larvae. Limnol Oceanogr 47(4):943–952CrossRefGoogle Scholar
  39. Nakagawa Y, Endo Y, Taki K (2002) Contributions of heterotrophic and autotrophic prey to the diet of euphausiid, Euphausia pacifica in the coastal waters off northeastern Japan. Polar Biosci 15:52–65Google Scholar
  40. Nichols DS, Nichols PD, Sullivan CW (1993) Fatty acid, sterol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarct Sci 5(3):271–278. doi: https://doi.org/10.1017/S0954102093000367 CrossRefGoogle Scholar
  41. Nicol S, de la Mare W (1993) Ecosystem management and the Antarctic krill. Am Sci 81:36–47Google Scholar
  42. Ohman MD (1984) Omnivory by Euphausia pacifica: the role of copepod prey. Mar Ecol Prog Ser 19:125–131. doi: https://doi.org/10.3354/meps019125 CrossRefGoogle Scholar
  43. Pakhomov EA, Perissinotto R (1996) Antarctic nertic krill Euphausia crystallorophias: spatio-temporal distribution, growth and grazing rates. Deep Sea Res Part I Oceanogr Res Pap 43:59–87. doi: https://doi.org/10.1016/0967-0637(95)00094-1 CrossRefGoogle Scholar
  44. Pond D, Watkins J, Priddle J, Sargent J (1995) Variation in the lipid content and composition of Antarctic krill Euphausia superba at South Georgia. Mar Ecol Prog Ser 117:49–57. doi: https://doi.org/10.3354/meps117049 CrossRefGoogle Scholar
  45. Quetin LB, Ross RM (1991) Behavioural and physiological characteristics of the Antarctic krill, Euphausia superba. Am Zool 31:49–63CrossRefGoogle Scholar
  46. Quetin LB, Ross RM, Clarke A (1994) Krill energetics: seasonal and environmental aspects of the physiology of Euphausia superba. In: El-Sayed SZ (ed) Southern Ocean ecology: the BIOMASS perspective. Cambridge University Press, Cambridge, pp 165–184Google Scholar
  47. Ross RM, Quetin LB, Newberger T, Oakes SA (2004) Growth and behavior of marvel krill (Euphausia superba) under the ice in late winter 2001 west of the Antarctic Peninsula. Deep Sea Res Part II Top Stud Oceanogr 51:2169–2184. doi: https://doi.org/10.1016/j.dsr2.2004.07.001 CrossRefGoogle Scholar
  48. Saito H, Kotani Y, Keriko JM, Xue C, Taki K, Ishihara K, Ueda T, Miyata S (2002) High levels of n-3 polyunsaturated fatty acids in Euphausia pacifica and its role as a source of dosahexaenoic and icosapentaenoic acids for higher trophic levels. Mar Chem 78:9–28. doi: https://doi.org/10.1016/S0304-4203(02)00005-1 CrossRefGoogle Scholar
  49. Shaw CT, Feinberg LR, Peterson WT (2004) Molting and growth rates of two species of euphausiids off the Oregon Coast: seasonal, spatial and life stage differences. ASLO/TOS Ocean Research Conference, HonoluluGoogle Scholar
  50. Siegel V (1987) Age and growth of Antarctic Euphasiacea (Crustacea) under natural conditions. Mar Biol (Berl) 96:483–495. doi: https://doi.org/10.1007/BF00397966 CrossRefGoogle Scholar
  51. Smiles MC, Pearcy WG (1971) Size, structure and growth of Euphausia pacifica off the Oregon coast. Fish Bull (Wash D C) 69:79–86. doi: https://doi.org/10.1126/science.174.4004.79 CrossRefGoogle Scholar
  52. Stübing D, Hagen W (2003) Fatty acid biomarker ratios-suitable trophic indicators in Antarctic euphausiids? Polar Biol 26:774–782. doi: https://doi.org/10.1007/s00300-003-0550-8 CrossRefGoogle Scholar
  53. Tanasichuk RW (1998a) Interannual variations in the population biology and productivity of the euphausiid, Euphausia pacifica in Barkely Sound, Canada, with special reference to the 1992 and 1993 warm ocean years. Mar Ecol Prog Ser 173:163–180. doi: https://doi.org/10.3354/meps173163 CrossRefGoogle Scholar
  54. Tanasichuk RW (1998b) Interannual variations in the population biology and productivity of the euphausiid, Thysanoessa spinifera in Barkely Sound, Canada, with special reference to the 1992 and 1993 warm ocean years. Mar Ecol Prog Ser 173:181–195. doi: https://doi.org/10.3354/meps173181 CrossRefGoogle Scholar
  55. Virtue P, Nichols PD, Nicol S, Hosie GW (1996) Reproductive trade-off in male Antarctic krill, Euphausia superba. Mar Biol (Berl) 126:521–527. doi: https://doi.org/10.1007/BF00354634 CrossRefGoogle Scholar
  56. Volkman JK, Everitt DA, Allen DI (1986) Some analyses of lipid classes in marine organisms, sediments and seawater using thin-layer chromatography-flame ionization detection. J Chromatogr A 356:147–162. doi: https://doi.org/10.1016/S0021-9673(00)91474-2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Se-Jong Ju
    • 1
  • Hyung-Ku Kang
    • 2
  • Woong Seo Kim
    • 3
  • H. Rodger Harvey
    • 4
  1. 1.Deep-sea and Marine Georesources Research DepartmentKorea Ocean Research and Development InstituteAnsan, SeoulRepublic of Korea
  2. 2.Marine Living Resources Research DepartmentKorea Ocean Research and Development InstituteAnsan, SeoulRepublic of Korea
  3. 3.Yeosu Exposition Supporting Task Force TeamKorea Ocean Research and Development InstituteAnsan, SeoulRepublic of Korea
  4. 4.Chesapeake Biological LaboratoryThe University of Maryland Center for Environmental ScienceSolomonsUSA

Personalised recommendations