Skip to main content
Log in

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

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackman RG, Tocher DS, McLachlan J (1968) Marine phytoplankter fatty acids. J Fish Res Bd Can 25:1603–1620

    Article  CAS  Google Scholar 

  • Arashkevich EG (1977) Duration of food digestion in marine copepods. Pol Arch Hydrobiol 24 : (Suppl) 431–438

    Google Scholar 

  • Atkinson A (1994) Diets and feeding selectivity among the epipelagic copepod community near South Georgia in summer. Polar Biol 14:551–560

    Article  Google Scholar 

  • 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 6:123–129

    Article  CAS  Google Scholar 

  • Bell MV, Sargent JR (1996) Lipid nutrition and fish recruitment. Mar Ecol Prog Ser 134:315–316

    Article  Google Scholar 

  • Bligh EG, Dyer WG (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917

    Article  CAS  Google Scholar 

  • Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biol 38:483–499

    Article  CAS  Google Scholar 

  • 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 31:267–278

    Article  Google Scholar 

  • Chu F-LE, Greaves J (1991) Metabolism of palmitic, linoleic, and linolenic acids in adult oysters, Crassostrea virginica. Mar Biol 110:5229–236

    Article  Google Scholar 

  • Chu F-LE, Ozkizilcik S (1995) Lipid and fatty acid composition of striped bass (Morone saxatilis) larvae during development. Comp Biochem Physiol 111:665–674

    Article  Google Scholar 

  • 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 19:273–278

    Article  Google Scholar 

  • 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):860–867

    Article  CAS  Google Scholar 

  • 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 226:497–509

    CAS  Google Scholar 

  • 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 27:1–18

    Article  CAS  Google Scholar 

  • 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 5:161–177

    Google Scholar 

  • Goad LJ (1981) Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl Chem 51:837–852

    Article  Google Scholar 

  • 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 182:97–110

    Article  CAS  Google Scholar 

  • Gurr MI, Harwood JL, Frayn KN (Eds) (2002) Lipid biochemistry. Blackwell , Oxford

    Book  Google Scholar 

  • 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 44:189–193

    Article  CAS  Google Scholar 

  • Jónasdóttir SH (1994) Effect of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Mar Biol 101:67–81

    Article  Google Scholar 

  • Jónasdóttir SH, Kiørboe T (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Mar Biol 125:743–750

    Article  Google Scholar 

  • Kattner G, Krause M, Trahms J (1981) Lipid composition of some typical North Sea copepods. Mar Ecol Prog Ser 4:69–74

    Article  CAS  Google Scholar 

  • 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 135:191–198

    Article  Google Scholar 

  • 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 274:199–208

    Article  Google Scholar 

  • 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 52:297–304

    Article  Google Scholar 

  • Kleppel GS, Burkart CA, Houchin L (1998) Nutrition and their regulation of egg production in the calanoid copepod Acartia tonsa. Limnol Oceanogr 43: 1000–1007

    Article  Google Scholar 

  • 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 170:169–187

    Article  Google Scholar 

  • 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 259:85–107

    Article  CAS  Google Scholar 

  • 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 204:65–77

    Article  Google Scholar 

  • Marty Y, Delaunay F, Moal J, Samain JF (1992) Change in the fatty acid composition of Pecten maximus. J Exp Mar Biol Ecol 163:221–34

    Article  CAS  Google Scholar 

  • Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579

    Article  CAS  Google Scholar 

  • Metcalfe LD, Schmitz AA (1961) The rapid preparation of fatty acid esters for gas chromatography analysis. Anal Chem 33:363–364

    Article  CAS  Google Scholar 

  • Moreno JJ, de Moreno JEA, Brenner RR (1979) Fatty acid metabolism in the calanoid copepod Paracalanus parvus: 1. polyunsaturated fatty acids. Lipids 14:313–322

    Article  CAS  Google Scholar 

  • 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 70:249–262

    Article  CAS  Google Scholar 

  • 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 427:69–72

    Article  Google Scholar 

  • 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 163:249–259

    Article  Google Scholar 

  • Norsker NH, Støttrup J (1994) The importance of dietary HUFAs for fecundity and PUFA content in the harpacticoid, Tisbe holothuriae Humes. Aquaculture 125:155–166

    Article  CAS  Google Scholar 

  • 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 33:201–205

    Article  Google Scholar 

  • Rainuzzo JR, Reitan KI, Olsen Y (1997) The significance of lipids at early stages of marine fish: a review. Aquaculture 155:103–115

    Article  CAS  Google Scholar 

  • 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 149–212

    Google Scholar 

  • 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 491–533

    Google Scholar 

  • 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 143:361–378

    Article  CAS  Google Scholar 

  • 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:451–457

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 141:87–105

    Article  Google Scholar 

  • Sul DG, Erwin JA (1997) The membrane lipids of the marine ciliated protozoan Parauronema acutum. Biochim Biophys Acta 1345:162–171

    Article  CAS  Google Scholar 

  • 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 318:85–98

    Article  Google Scholar 

  • 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 179:71–79

    Article  CAS  Google Scholar 

  • Tang KW, Jakobsen HH, Visser AW (2001) Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: Feeding, growth and trophic interactions among grazers. Limnol Oceanogr 46:1860–1870

    Article  Google Scholar 

  • Watanabe T (1993) Importance of docosahexaenoic acid in marine larval fish. J World Aquacult Soc 24:152–161

    Article  Google Scholar 

  • Zhukova NV, Kharlamenko VI (1999) Sources of essential fatty acids in the marine microbial loop. Aquat Microb Ecol 17:153–157

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fu-Lin E. Chu.

Additional information

Communicated by J. P. Grassle, New Brunswick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Veloza, A.J., Chu, FL.E. & Tang, K.W. Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepod Acartia tonsa . Marine Biology 148, 779–788 (2006). https://doi.org/10.1007/s00227-005-0123-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0123-1

Keywords

Navigation