Marine Biology

, Volume 148, Issue 4, pp 779–788 | Cite as

Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepod Acartia tonsa

  • Adriana J. Veloza
  • Fu-Lin E. ChuEmail author
  • Kam W. Tang
Research Article


To test whether heterotrophic protists modify precursors of long chain n−3 polyunsaturated fatty acids (LCn−3PUFAs) present in the algae they eat, two algae with different fatty acid contents (Rhodomonas salina and Dunaliella tertiolecta) were fed to the heterotrophic protists Oxyrrhis marina Dujardin and Gyrodinium dominans Hulbert. These experiments were conducted in August 2004. Both predators and prey were analyzed for fatty acid composition. To further test the effects of trophic upgrading, the calanoid copepod Acartia tonsa Dana was fed R. salina, D. tertiolecta, or O. marina that had been growing on D. tertiolecta (OM-DT) in March 2005. Our results show that trophic upgrading was species-specific. The presence of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) in the heterotrophic protists despite the lack of these fatty acids in the algal prey suggests that protists have the ability to elongate and desaturate 18:3 (n−3), a precursor of LCn−3PUFAs, to EPA and/or DHA. A lower content of these fatty acids was detected in protists that were fed good-quality algae. Feeding experiments with A. tonsa showed that copepods fed D. tertiolecta had a significantly lower content of EPA and DHA than those fed OM-DT. The concentration of EPA was low on both diets, while DHA content was highest in A. tonsa fed R. salina and OM-DT. These results suggest that O. marina was able to trophically upgrade the nutritional quality of the poor-quality alga, and efficiently supplied DHA to the next trophic level. The low amount of EPA in A. tonsa suggests EPA may be catabolized by the copepod.


Dunaliella Heterotrophic Dinoflagellate Heterotrophic Protist Dunaliella Tertiolecta Paracalanus Parvus 
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.



This study was supported by NOAA-CMER awards NA03NMF4550382 and NA04NMF4550390, and by Sigma Xi Grants In Aid of Research. The authors are grateful for Dr. Eric Lund’s advice and help in lipid analysis, GC operation and editing the revised version of this manuscript. The authors thank Mrs. Georgetta Constantin for assistance in lipid analyses. Contribution no. 2698 by the Virginia Institute of Marine Science, College of William and Mary.


  1. Ackman RG, Tocher DS, McLachlan J (1968) Marine phytoplankter fatty acids. J Fish Res Bd Can 25:1603–1620CrossRefGoogle Scholar
  2. Arashkevich EG (1977) Duration of food digestion in marine copepods. Pol Arch Hydrobiol 24 : (Suppl) 431–438Google Scholar
  3. Atkinson A (1994) Diets and feeding selectivity among the epipelagic copepod community near South Georgia in summer. Polar Biol 14:551–560CrossRefGoogle Scholar
  4. Barclay WR, Meager KM, Abril JR (1994) Heterotrophic production of long chain omega-3 fatty acids utilizing algae and algae-like microorganisms. J Appl Phycol 6:123–129CrossRefGoogle Scholar
  5. Bell MV, Sargent JR (1996) Lipid nutrition and fish recruitment. Mar Ecol Prog Ser 134:315–316CrossRefGoogle Scholar
  6. Bligh EG, Dyer WG (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917CrossRefGoogle Scholar
  7. Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biol 38:483–499CrossRefGoogle Scholar
  8. Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31:267–278CrossRefGoogle Scholar
  9. Chu F-LE, Greaves J (1991) Metabolism of palmitic, linoleic, and linolenic acids in adult oysters, Crassostrea virginica. Mar Biol 110:5229–236CrossRefGoogle Scholar
  10. Chu F-LE, Ozkizilcik S (1995) Lipid and fatty acid composition of striped bass (Morone saxatilis) larvae during development. Comp Biochem Physiol 111:665–674CrossRefGoogle Scholar
  11. Desvilletes C, Bourdier G, Breton JC (1997) On the occurrence of a possible bioconversion of linolenic acid into docosahexaenoic acid by the copepod Eucyclops serrulatus fed on phytoplankton. J Plankton Res 19:273–278CrossRefGoogle Scholar
  12. Ederington MC, McManus GB, Harvey HR (1995) Trophic transfer of fatty acids, sterols, and a triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol Oceanogr 40(5):860–867CrossRefGoogle Scholar
  13. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  14. Fraser AJ, Sargent JR (1989) Formation and transfer of fatty acids in an enclosed marine food chain comprising phytoplankton, zooplankton and herring (Clupea harengus L.) larvae. Mar Chem 27:1–18CrossRefGoogle Scholar
  15. Gifford DJ, Dagg MJ (1991) The microzooplankton–mesozooplankton link: consumption of planktonic protozoa by the calanoid copepods Acartia tonsa Dana and Neocalanus plumchrus Murkukawa. Mar Microb Food Webs 5:161–177Google Scholar
  16. Goad LJ (1981) Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl Chem 51:837–852CrossRefGoogle Scholar
  17. Graeve M, Kattner G, Hagen W (1994) Diet induced changes in the fatty acid composition of Arctic herbivorous copepods: experimental evidence of trophic markers. J Exp Mar Biol Ecol 182:97–110CrossRefGoogle Scholar
  18. Gurr MI, Harwood JL, Frayn KN (Eds) (2002) Lipid biochemistry. Blackwell , OxfordCrossRefGoogle Scholar
  19. Harvey HR, Ederington MC, McManus GB (1997) Lipid composition of the marine ciliates Pleuronema sp. and Fabrea salina: shifts in response to changes in diet. J Eukaryot Microbiol 44:189–193CrossRefGoogle Scholar
  20. Jónasdóttir SH (1994) Effect of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Mar Biol 101:67–81CrossRefGoogle Scholar
  21. Jónasdóttir SH, Kiørboe T (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Mar Biol 125:743–750CrossRefGoogle Scholar
  22. Kattner G, Krause M, Trahms J (1981) Lipid composition of some typical North Sea copepods. Mar Ecol Prog Ser 4:69–74CrossRefGoogle Scholar
  23. Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar Biol 135:191–198CrossRefGoogle Scholar
  24. Klein Breteler WCM, Koski M, Rampen S (2004) Role of essential lipids in copepod nutrition: no evidence of trophic upgrading of food quality by a marine ciliate. Mar Ecol Prog Ser 274:199–208CrossRefGoogle Scholar
  25. Kleppel GS, Burkart CA (1995) Egg production and the nutritional environment of Acartia tonsa: the role of food quality in copepod nutrition. ICES J Mar Sci 52:297–304CrossRefGoogle Scholar
  26. Kleppel GS, Burkart CA, Houchin L (1998) Nutrition and their regulation of egg production in the calanoid copepod Acartia tonsa. Limnol Oceanogr 43: 1000–1007CrossRefGoogle Scholar
  27. Koski M, Klein Breteler W, Schogt N (1998) Effect of food quality on rate of growth and development of the pelagic copepod Pseudocalanus elongatus (Copepoda, Calanoida). Mar Ecol Prog Ser 170:169–187CrossRefGoogle Scholar
  28. Lacoste A, Poulet SA, Cueff A, Kattner G, Ianora A, Laabir M (2001) New evidence of the copepod maternal food effects on reproduction. J Exp Mar Biol Ecol 259:85–107CrossRefGoogle Scholar
  29. Levinsen H, Turner JT, Nielsen TG, Hansen BW (2000) On the trophic coupling between protists and copepods in arctic marine ecosystems. Mar Ecol Prog Ser 204:65–77CrossRefGoogle Scholar
  30. Marty Y, Delaunay F, Moal J, Samain JF (1992) Change in the fatty acid composition of Pecten maximus. J Exp Mar Biol Ecol 163:221–34CrossRefGoogle Scholar
  31. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579CrossRefGoogle Scholar
  32. Metcalfe LD, Schmitz AA (1961) The rapid preparation of fatty acid esters for gas chromatography analysis. Anal Chem 33:363–364CrossRefGoogle Scholar
  33. Moreno JJ, de Moreno JEA, Brenner RR (1979) Fatty acid metabolism in the calanoid copepod Paracalanus parvus: 1. polyunsaturated fatty acids. Lipids 14:313–322CrossRefGoogle Scholar
  34. Morris RJ, McCartney MJ, Robinson GA (1983) Studies of a spring phytoplankton bloom in an enclosed experimental ecosystem. I. Biochemical changes in relation to the nutrient chemistry of water. J Exp Mar Biol Ecol 70:249–262CrossRefGoogle Scholar
  35. Müller-Navarra DC, Brett MT, Park S, Chandra S, Ballantyne AP, Zorita E, Goldman CR (2004) Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 427:69–72CrossRefGoogle Scholar
  36. Nanton DA, Castell JD (1998) The effects of dietary fatty acids on the fatty acid composition of the harpacticoid copepod, Tisbe sp., for use as a live food for marine fish larvae. Aquaculture 163:249–259CrossRefGoogle Scholar
  37. Norsker NH, Støttrup J (1994) The importance of dietary HUFAs for fecundity and PUFA content in the harpacticoid, Tisbe holothuriae Humes. Aquaculture 125:155–166CrossRefGoogle Scholar
  38. Park S, Brett MT, Müller-Navarra DC, Shin SC, Liston AM, Goldman CR (2003) Heterotrophic nanoflagellates and increased essential fatty acids during Mycrocistis decay. Aquat Microb Ecol 33:201–205CrossRefGoogle Scholar
  39. Rainuzzo JR, Reitan KI, Olsen Y (1997) The significance of lipids at early stages of marine fish: a review. Aquaculture 155:103–115CrossRefGoogle Scholar
  40. Sargent JR (1976) The structure, metabolism, and function of lipids in marine organisms. In: Malins C, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology. Academic Press, London, pp 149–212Google Scholar
  41. Sargent JR, Whittle KJ (1981) Lipids and hydrocarbons in the marine food web. In: Longhurst AR (eds) Analysis of marine ecosystems. Academic Press, London, pp 491–533Google Scholar
  42. Soudant P, Marty Y, Moal J, Robert R, Quere C, Le Coz JR, Samain JF (1996) Effect of food fatty acid and sterol quality on Pecten maximus gonad composition and reproduction process. Aquaculture 143:361–378CrossRefGoogle Scholar
  43. Soudant P, Le Coz JR, Marty Y, Moal J, Robert R, Samain JF (1998) Incorporation of microalgae sterols by scallop Pecten maximus (L.) larvae. Comp Biochem Physiol 119A:451–457CrossRefGoogle Scholar
  44. Strathmann RR (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol Oceanogr 12:411–418CrossRefGoogle Scholar
  45. Støttrup JG, Jensen J (1990) Influence of algal diet on feeding and egg production of the calanoid copepod Acartia tonsa Dana. J Exp Mar Biol Ecol 141:87–105CrossRefGoogle Scholar
  46. Sul DG, Erwin JA (1997) The membrane lipids of the marine ciliated protozoan Parauronema acutum. Biochim Biophys Acta 1345:162–171CrossRefGoogle Scholar
  47. Tang KW, Taal M (2005) Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J Exp Mar Biol Ecol 318:85–98CrossRefGoogle Scholar
  48. Tang KW, Dam HG, Visscher PT, Fenn TD (1999) Dimethylsulfoniopropionate (DMSP) in marine copepods and its relation with diets and salinity. Mar Ecol Prog Ser 179:71–79CrossRefGoogle Scholar
  49. Tang KW, Jakobsen HH, Visser AW (2001) Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: Feeding, growth and trophic interactions among grazers. Limnol Oceanogr 46:1860–1870CrossRefGoogle Scholar
  50. Watanabe T (1993) Importance of docosahexaenoic acid in marine larval fish. J World Aquacult Soc 24:152–161CrossRefGoogle Scholar
  51. Zhukova NV, Kharlamenko VI (1999) Sources of essential fatty acids in the marine microbial loop. Aquat Microb Ecol 17:153–157CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Adriana J. Veloza
    • 1
  • Fu-Lin E. Chu
    • 1
    Email author
  • Kam W. Tang
    • 1
  1. 1.Virginia Institute of Marine ScienceGloucester PointUSA

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