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.
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
Arashkevich EG (1977) Duration of food digestion in marine copepods. Pol Arch Hydrobiol 24 : (Suppl) 431–438
Atkinson A (1994) Diets and feeding selectivity among the epipelagic copepod community near South Georgia in summer. Polar Biol 14:551–560
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
Bell MV, Sargent JR (1996) Lipid nutrition and fish recruitment. Mar Ecol Prog Ser 134:315–316
Bligh EG, Dyer WG (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917
Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biol 38:483–499
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
Chu F-LE, Greaves J (1991) Metabolism of palmitic, linoleic, and linolenic acids in adult oysters, Crassostrea virginica. Mar Biol 110:5229–236
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
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
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
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
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
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
Goad LJ (1981) Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl Chem 51:837–852
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
Gurr MI, Harwood JL, Frayn KN (Eds) (2002) Lipid biochemistry. Blackwell , Oxford
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
Jónasdóttir SH (1994) Effect of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Mar Biol 101:67–81
Jónasdóttir SH, Kiørboe T (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Mar Biol 125:743–750
Kattner G, Krause M, Trahms J (1981) Lipid composition of some typical North Sea copepods. Mar Ecol Prog Ser 4:69–74
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
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
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
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
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
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
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
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
Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579
Metcalfe LD, Schmitz AA (1961) The rapid preparation of fatty acid esters for gas chromatography analysis. Anal Chem 33:363–364
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
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
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
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
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
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
Rainuzzo JR, Reitan KI, Olsen Y (1997) The significance of lipids at early stages of marine fish: a review. Aquaculture 155:103–115
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
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
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
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
Strathmann RR (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol Oceanogr 12:411–418
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
Sul DG, Erwin JA (1997) The membrane lipids of the marine ciliated protozoan Parauronema acutum. Biochim Biophys Acta 1345:162–171
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
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
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
Watanabe T (1993) Importance of docosahexaenoic acid in marine larval fish. J World Aquacult Soc 24:152–161
Zhukova NV, Kharlamenko VI (1999) Sources of essential fatty acids in the marine microbial loop. Aquat Microb Ecol 17:153–157
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
Corresponding author
Additional information
Communicated by J. P. Grassle, New Brunswick
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-005-0123-1