Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Ecological implications of fecal pellets produced by the Antarctic krill Euphausia superba in the Antarctic Ocean

Abstract

Organic analyses and electron microscopic observations on fecal pellets produced by the Antarctic krill Euphausia superba Dana showed that krill fed on choanoflagellates, the abundant heterotrophic flagellate in the Antarctic Ocean. Two new pathways of organic materials in the Antarctic ecosystem are proposed: (1) a new food chain including non-living particulate and dissolved organics, and bacteria-choanoflagellate-krill-vertebrate, which coexists with the traditional diatom-krill-vertebrate food chain; (2) non-phytoplanktonic organic materials in surface waters are transferred into choanoflagellates and are transported to deep water as fecal pellets which are still useful as nutrition for other organisms there.

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

Literature cited

  1. Anderson, P. and T. Fenchel: Bacterivory by microheterotrophic flagellates in sea water samples. Limnol. Oceanogr. 30, 198–202 (1985)

  2. Barkley, E.: Nahrung und Filterapparat des Walkrebschens Euphausia superba Dana. Z. Fish. 1, 65–156 (1940)

  3. Beasley, T. M., M. Heyraud, J. J. W. Higgo, R. D. Cherry and S. W. Fowler: 210Po and 210Pb in zooplankton fecal pellets. Mar. Biol. 44, 325–328 (1978)

  4. Boothe, P. N. and G. A. Knauer: The possible importance of fecal materials in the biological amplification of trace and heavy metals. Limnol. Oceanogr. 17, 270–274 (1972)

  5. Buck, K. R.: A study of choanoflagellates (Acanthoecidae) from the Weddell Sea, including a description of Diaphanoeca multiannulata n.sp. J. Protozool. 28, 47–54 (1981)

  6. Buck, K. R. and D. L. Garrison: Protists from the ice edge region of the Weddel Sea. Deep-Sea Res. 30, 1261–1277 (1983)

  7. Cauwet, G.: Non-living particulate matter. In: Marine organic chemistry, pp 71–89. Ed. by E. K. Duursma and R. Dawson. Amsterdam: Elsevier Scientific Pub. Co. 1981

  8. Chuecas, L. and J. P. Riley: Component fatty acids of the total lipids of some marine phytoplankton. J. mar. biol. Ass. UK. 49, 97–116 (1969)

  9. Deflandre, G.: Sur la présence de Parvicorbicula n.g. socialis (Meunier) dans le plancton de l'Antarctique (Terre Adélie). Rev. Algol. 5, 183–189 (1960)

  10. DeMort, C. L., R. Lowry, I. Tinsley and H. K. Phinney: The biochemical analysis of some estuarine phytoplankton species. I. Fatty acid composition. J. Phycol. 8, 211–216 (1972)

  11. Elder, D. L. and S. W. Fowler: Polychlorinated biphenyls: penetration into the deep ocean by zooplankton fecal pellet transport. Science, Wash., D. C. 197, 459–461 (1977)

  12. Fenchel, T.: Ecology of heterotrophic micro-flagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9, 35–42 (1982)

  13. Folch, J., M. Lees and G. H. Sloane Stanley: A simple method for the isolation and purification of total lipid from animal tissues. J. Biol. Chem. 226a, 497–509 (1957)

  14. Fowler, S. W.: Trace elements in zooplankton particulate products. Nature, Lond. 269, 51–53 (1977)

  15. Fowler, S. W. and L. F. Small: Sinking rates of euphausiid fecal pellets. Limnol. Oceanogr. 17, 293–296 (1972)

  16. Frankenberg, D. and K. L. Smith, Jr.: Comprophagy in marine animals. Limnol. Oceanogr. 12, 443–450 (1967)

  17. Frankenberg, D., S. L. Cole and R. E. Johannes: The potential trophic significance of Callianassa major fecal pellet. Limnol. Oceanogr. 12, 113–120 (1967)

  18. Gold, K., R. M. Pfister and V. R. Liguori: Axenic cultivation and electron microscopy of two species of choanoflagellida. J. Protozool. 17, 210–212 (1970)

  19. Haas, L. W. and K. L. Webb: Nutritional mode of several nonpigmented microflagellates from the York River Estuary. J. exp. mar. Biol. Ecol. 39, 125–134 (1979)

  20. Hara, S., E. Tanoue, M. Zenimoto, Y. Komaki and E. Takahashi: Heterotrophic protists along the transect of 75°E in the Southern Ocean. Mem. Nat. Inst. Polar Res., Special issue 40, 69–80 (1986)

  21. Hardy, A. C.: Observations on the uneven distribution of oceanic plankton. Discovery Rep. 11, 511–538 (1936)

  22. Hempel, G.: Antarctic marine food webs. In: Antarctic nutrient cycles and food webs, pp 266–270. Ed. by. W. R. Siegfried, P. R. Condy and R. M. Law: Berlin, Heidelberg: Springer Verlag 1985

  23. Hewes, C. D., O. Holm-Hansen and E. Sakshaug: Alternate carbon pathways at lower trophic levels in the antarctic food web. In: Antarctic nutrient cycles and food webs, pp 277–283. Ed. by W. R. Siegfried, P. R. Condy and R. M. Laws. Berlin, Heidelberg: Springer Verlag 1985

  24. Holm-Hansen, O.: Nutrient cycles in antarctic marine ecosystems. In: Antarctic nutrient cycles and food webs. pp 6–10. Ed. by W. R. Siegfried, P. R. Condy and R. M. Laws. Berlin, Heidelberg: Springer Verlag 1985

  25. Honjo, S.: Coccoliths: production, transportation and sedimentation. Mar Micropaleont. 1, 65–79 (1976)

  26. Honjo, S. and M. R. Roman: Marine copepod fecal pellets: production, preservation and sedimentation. J. mar. Res. 36, 45–57 (1978)

  27. Johannes, R. E. and M. Satomi: Composition and nutritive value of fecal pellets of a marine crustacean. Limnol. Oceanogr. 11, 191–197 (1966)

  28. Joint, I. R. and R. J. Morris: The role of bacteria in the turnover of organic matter in the sea. Oceanogr. mar. biol. Ann. Rev. 20, 65–118 (1982)

  29. Kates, M. and B. E. Volcani: Lipid components of diatoms. Biochim. biophys. Acta 116, 264–278 (1966)

  30. Kato, M., S. Segawa, E. Tanoue and M. Murano: Filtering and ingestion rates of the antarctic krill, Euphausia superba Dana. Trans. Tokyo Univ. Fish. 5, 167–175 (1982)

  31. Kawamura, A.: Food habits of Euphausia superba and diatom community. In: BIOMASS, vol. 2, pp 65–68. Ed. by S.Z. ElSayed. Cambridge: Scott Polar Res. Inst. 1981

  32. Laval, M.: Ultrastructure et mode de nutrition du choanoflagelle Salpingoeca pelagica sp. nov. Comparison avec les choanocytes des spongaires. Prostistologica 7, 325–336 (1971)

  33. Leadbeater, B. S. C. and C. Morton: A microscopical study of marine species of Codosiga James-Clark (Choanoflagellata) with special reference to the ingestion of bacteria. Biol. J. Linn. Soc. 6, 337–347 (1974)

  34. Lightheart, B.: Planktonic and benthic bacteriovorous protozoa at eleven stations in Puget Sound and adjacent Pacific ocean. J. Fish. Res. Bd Can. 26, 299–304 (1969)

  35. Manton, I., J. Sutherland and B. S. C. Leadbeater: Further observations on the fine structure of marine collared flagellates (Choanoflagellata) from arctic Canada and west Greenland: species of Parvicorbicula and Pleurasiga. Can. J. Bot. 54, 1932–1955 (1976)

  36. Marchant, H. J.: Choanoflagellates in the antarctic marine food chain. In: Antarctic nutrient cycles and food webs, pp 271–276, Ed. by W. R. Siegfried, P. R. Condy and R. M. Laws. Berlin, Heidelberg: Springer Verlag 1985

  37. Marr, J.: The natural history and geography of the Antarctic krill (Euphausia superba Dana). Discovery Rep. 32, 33–464 (1962)

  38. Metcalfe, L. D., A. A. Schmitz and J. R. Pelka: Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Anal. Chem. 38, 514–515 (1966)

  39. Meyer, M. A. and S. Z. El-Sayed: Grazing of Euphausia superba Dana on natural plankton population. Polar Biol. 1, 193–197 (1983)

  40. Morris, D. J.: Filtration rates in Euphausia superba: under or overestimates? J. Crust. Biol. 4, (Spec. No 1), 185–197 (1984)

  41. Nemoto, T.: History of research into the food and feeding of euphausiids. Proc. R. Soc. Edinburgh 73, 259–265 (1971/1972)

  42. Newell, R.: The role of detritus in the nutrition of two marine deposit feeders, the prosobranch Hydrobio ulvae and the bivalve Macoma baltica. Proc. Zool. Soc. Lond. 144, 25–45 (1965)

  43. Oser, B. L.: Method for integrating essential amino acid content in the nutritional evaluation of protein. J. Am. Diet. Ass. 27, 396–402 (1951)

  44. Osterberg, C. A., G. Carey and H. Curl: Acceleration of sinking rates of radionuclides in the ocean. Nature, Lond. 200, 1276–1277 (1963)

  45. Paffenhöfer, G. A. and S. C. Knowles: Ecological implications of fecal pellet size, production and consumption by copepods. J. mar. Res. 37, 35–49 (1979)

  46. Pavlov, V. Y.: On the physiology of feeding in Euphausia superba. Proc. Acad. Sci. USSR. 196, 147–150 (1971)

  47. Prahl, F. G., G. Eglinton, E. D. S. Corner and S. C. M. O'Hara: Copepod fecal pellets as a source of dihydrophytol in marine sediments. Science, Wash., D. C. 224, 1235–1237 (1984)

  48. Quetin, L. B. and R. M. Ross: Feeding by Antarctic krill, Euphausia superba: does size matter? In: Antarctic nutrient cycles and food webs, pp 373–377. Ed. by W. R. Siegfried, P. R. Condy and R. M. Laws. Berlin, Heidelberg: Springer Verlag 1985

  49. Rhead, M. M., G. Eglinton, G. H. Draffan and P. J. England: Conversion of oleic acid to saturated fatty acids in seven estuary sediments. Nature, Lond. 232, 327–330 (1971)

  50. Schrader, H. J.: Fecal pellets: role in sedimentation of pelagic diatoms. Science, Wash., D. C. 174, 55–57 (1971)

  51. Sieburth, J.: Sea microbes, 491 pp. New York: Oxford University Press 1979

  52. Sieburth, J. and P. G. Davis: The role of heterotrophic nanoplankton in the grazing of planktonic bacteria in the Sargasso and Caribbean Seas. Ann. Inst. Oceanogr., Paris 58, 285–296 (1982)

  53. Silver, M. W., J. G. Michell and D. L. Ringo: Siliceous nanoplankton. II. Newly discovered cysts and abundant choanoflagellates from the Weddel Sea, Antarctica. Mar. Biol. 58, 211–217 (1980)

  54. Smayda, T. J.: Some measurements of the sinking rate of fecal pellets. Limnol. Oceanogr. 14, 612–625 (1969)

  55. Smayda, T. J.: Normal and accelerated sinking of phytoplankton in the sea. Mar. Geol. 11, 105–122 (1971)

  56. Sorokin, Y. I.: On the role of bacteria in the productivity of tropical oceanic waters. Int. Revue ges. Hydrobiol. 56, 1–48 (1971)

  57. Sorokin, Y. I.: Microheterotrophic organisms in marine ecosystems. In: Analysis of marine ecosystems, pp 293–342. Ed. by A. R. Longhurst. London: Academic Press 1981

  58. Strathmann, R. R.: Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceanogr. 12, 411–418 (1967)

  59. Takahashi, E.: Loricate and scale-bearing protists from Lützow-Holm Bay, Antarctica I. Species of the Acanthoecidae and the Centrohelida found at a site selected on the fast ice. Antarct. Rec. 73, 1–22

  60. Tanoue, E. and N. Handa: Vertical transport of organic materials in the northern North Pacific as determined by sediment trap experiment. Part 1. Fatty acid composition. J. Oceanogr. Soc. Japan 36, 231–235 (1980)

  61. Tanoue, E., N. Handa and M. Kato: Horizontal and vertical distribution of particulate organic matter in the Pacific sector of the Antarctic Ocean. Trans. Tokyo Univ. Fish. 5, 65–83 (1982a)

  62. Tanoue, E., N. Handa and H. Sakugawa: Difference of the chemical composition of organic matter between fecal pellet of Euphausia superba and its feed, Dunaliella tertiolecta. Trans. Tokyo Univ. Fish. 5, 189–196 (1982b)

  63. Turner, J. T.: Sinking rates of fecal pellets from the marine copepod Pontella meadii. Mar. Biol. 40, 249–259 (1977)

  64. Wiebe, P. H., S. H. Boyd and C. Winget: Particulate matter sinking to the deep sea floor at 2 000 m in the tongue of the ocean, Bahamas, with a description of a new sedimentation trap. J. mar. Res. 34, 341–354 (1976)

  65. Williams, P. J. L.: Biological and chemical aspects of dissolved organic matter in seawater. In: Chemical oceanography 2, pp 301–363. Ed. by J. P. Riley and G. Skirrow. London: Academic Press 1975

Download references

Author information

Additional information

Communicated by M. Anraku, Hiroshima

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tanoue, E., Hara, S. Ecological implications of fecal pellets produced by the Antarctic krill Euphausia superba in the Antarctic Ocean. Mar. Biol. 91, 359–369 (1986). https://doi.org/10.1007/BF00428630

Download citation

Keywords

  • Surface Water
  • Organic Material
  • Deep Water
  • Food Chain
  • Microscopic Observation