Skip to main content

Advertisement

SpringerLink
Log in

Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir

  • Ecosystem ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

One of the central paradigms of ecology is that only about 10% of organic carbon production of one trophic level is incorporated into new biomass of organisms of the next trophic level. Many of energy-yielding compounds of carbon are designated as ‘essential’, because they cannot be synthesized de novo by consumers and must be obtained with food, while they play important structural and regulatory functions. The question arises: are the essential compounds transferred through trophic chains with the same efficiency as bulk carbon? To answer this question, we measured gross primary production of phytoplankton and secondary production of zooplankton and content of organic carbon and essential polyunsaturated fatty acids of ω-3 family with 18–22 carbon atoms (PUFA) in the biomass of phytoplankton and zooplankton in a small eutrophic reservoir during two summers. Transfer efficiency between the two trophic levels, phytoplankton (producers) and zooplankton (consumers), was calculated as ratio of the primary production versus the secondary (zooplankton) production for both carbon and PUFA. We found that the essential PUFA were transferred from the producers to the primary consumers with about twice higher efficiency than bulk carbon. In contrast, polyunsaturated fatty acids with 16 carbon atoms, which are synthesized exclusively by phytoplankton, but are not essential for animals, had significantly lower transfer efficiency than both bulk carbon, and essential PUFA. Thus, the trophic pyramid concept, which implicitly implies that all the energy-yielding compounds of carbon are transferred from one trophic level to the next with the same efficiency of about on average 10%, should be specified for different carbon compounds.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahlgren G, Gustafsson IB, Boberg M (1992) Fatty acid content and chemical composition of freshwater microalgae. J Phycol 28:37–50

    Article  CAS  Google Scholar 

  • Ahlgren G, Goedkoop W, Markensten H, Sonesten L, Boberg M (1997) Seasonal variations in food quality for pelagic and benthic invertebrates in lake Erken—the role of fatty acids. Freshw Biol 38:555–570

    Article  CAS  Google Scholar 

  • Alimov AF (1989) An introduction to production hydrobiology. Gidrometeoizdat, Leningrad

    Google Scholar 

  • Aoki I (2006) Ecological pyramid of dissipation function and entropy production in aquatic ecosystems. Ecol Complex 3:104–108

    Article  Google Scholar 

  • Arts MT, Ackman RG, Holub BJ (2001) ‘‘Essential fatty acids’’ in aquatic ecosystems: a crucial link between diet and human health and evolution. Can J Fish Aquat Sci 58:122–137

    Article  CAS  Google Scholar 

  • Balushkina EV, Winberg GG (1979) Relation between mass and body size of plankton animals. In: Winberg GG (ed) General backgrounds for study of aquatic ecosystems. Nauka, Leningrad, pp 169–172

    Google Scholar 

  • Bell MV, Tocher DR (2009) Biosynthesis of polyunsaturated fatty acids in aquatic ecosystems: general pathways and new directions. In: Arts MT, Kainz M, Brett MT (eds) Lipids in aquatic ecosystems. Springer, New York, pp 211–236

    Chapter  Google Scholar 

  • Brett MT, Muller-Navarra DC, Ballantyne AP, Ravet JL, Goldman CR (2006) Daphnia fatty acid compostion reflects that of their diet. Limnol Oceanogr 51:2428–2437

    Article  CAS  Google Scholar 

  • Clesceri CE, Greenberg AE, Trussell RR (1989) Standard methods (for the examination of water and wastewater). American Public Health Association, American Water Works Association, Water Pollution Control Federation, Washington

    Google Scholar 

  • Cohen Z, Norman HA, Heimer YM (1995) Microalgae as a source of ω-3 fatty acids. In: Simopoulos AP (ed) Plants in human nutrition. World review of nutrition and dietetics, vol 77. Karger, Basel, pp 1–31

    Google Scholar 

  • Copeman LA, Parrish CC, Brown JA, Harel M (2002) Effects of docosahexaenoic, eicosapentaenoic, and arachidonic acids on the early growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture 210:285–304

    Article  CAS  Google Scholar 

  • DeMott WR, Gulati RD (1999) Phosphorus limitation in Daphnia: evidence from a long-term study of three hypereutrophic Dutch lakes. Limnol Oceanogr 44:1557–1564

    Article  CAS  Google Scholar 

  • Domergue F, Spiekermann P, Lerchl J, Beckmann C, Kilian O, Kroth PG, Boland W, Zahringer U, Heinz E (2003) New insights into Phaeodactylum tricornutum fatty acid metabolism. Cloning and functional characterization of plastidial and microsomal Δ12-fatty acid desaturases. Plant Physiol 131:1648–1660

    Article  CAS  PubMed  Google Scholar 

  • Gaevsky NA, Kolmakov VI, Popelnitsky VA, Gold VM, Dubovskaya OP (2000) Evaluation of the effect of light intensity on the measurement of the photosynthetic rate in plankton microalgae by the chlorophyll fluorescence method. Russ J Plant Physiol 47:820–825

    Article  Google Scholar 

  • Gaevsky NA, Zotina TA, Gorbaneva TB (2002) Vertical structure and photosynthetic activity of Lake Shira phytoplankton. Aquat Ecol 36:165–178

    Article  CAS  Google Scholar 

  • Gaevsky NA, Kolmakov VI, Anishchenko OV, Gorbaneva TB (2005) Using DCMU-fluorescence method for identification of dominating phytoplankton groups. J Appl Phycol 17:483–494

    Article  CAS  Google Scholar 

  • Garg ML, Wood LG, Singh H, Moughan PJ (2006) Means of delivering recommended levels of long chain n-3 polyunsaturated fatty acids in human diets. J Food Sci 71:R66–R71

    Article  CAS  Google Scholar 

  • Gerster H (1998) Can adults adequately convert α-linoleic acid (18:3n-3) to eicosapentaenoic acid (20:5n-3) and docosahexaenoic acid (22:6n-3)? Int J Vitamin Nutr Res 68:159–173

    CAS  Google Scholar 

  • Gladyshev MI, Emelianova AY, Kalachova GS, Zotina TA, Gaevsky NA, Zhilenkov MD (2000) Gut content analysis of Gammarus lacustris from a Siberian lake using biochemical and biophysical methods. Hydrobiologia 431:155–163

    Article  CAS  Google Scholar 

  • Gladyshev MI, Sushchik NN, Kolmakova A, Kalachova GS, Kravchuk ES, Ivanova EA, Makhutova ON (2007) Seasonal correlations of elemental and ω-3 PUFA composition of seston and dominant phytoplankton species in a eutrophic Siberian reservoir. Aquat Ecol 41:9–23

    Article  CAS  Google Scholar 

  • Gladyshev MI, Arts MT, Sushchik NN (2009) Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terrestrial ecosystems. In: Arts MT, Kainz M, Brett MT (eds) Lipids in aquatic ecosystems. Springer, New York, pp 179–209

    Chapter  Google Scholar 

  • Gladyshev MI, Krylov AV, Sushchik NN, Malin MI, Makhutova ON, Chalova IV, Kalacheva GS (2010a) Transfer of essential polyunsaturated fatty acids from an aquatic to terrestrial ecosystem through the fish–bird trophic pair. Doklady Biol Sci 431:121–123

    Article  CAS  Google Scholar 

  • Gladyshev MI, Sushchik NN, Makhutova ON, Dubovskaya OP, Kravchuk ES, Kalachova GS, Khromechek EB (2010b) Correlations between fatty acid composition of seston and zooplankton and effects of environmental parameters in a eutrophic Siberian reservoir. Limnologica 40:343–357

    CAS  Google Scholar 

  • Goulden CE, Place AR (1990) Fatty acid synthesis and accumulation rates in daphniids. J Exp Zool 256:168–178

    Article  CAS  Google Scholar 

  • Gutseit K, Berglund O, Graneli W (2007) Essential fatty acids and phosphorus in seston from lakes with contrasting terrestrial dissolved organic carbon content. Freshw Biol 52:28–38

    Article  CAS  Google Scholar 

  • Harwood JL (1996) Recent advances in the biosynthesis of plant fatty acids. Biochim Biophys Acta 1301:7–56

    PubMed  Google Scholar 

  • Heinz E (1993) Biosynthesis of polyunsaturated fatty acids. In: Moore TS (ed) Lipid metabolism in plants. CRC, Boca Raton, pp 34–89

    Google Scholar 

  • Hessen DO, Andersen T, Brettum P, Faafeng BA (2003) Phytoplankton contribution to sestonic mass and elemental ratios in lakes: implications for zooplankton nutrition. Limnol Oceanogr 48:1289–1296

    Article  CAS  Google Scholar 

  • Ishimaru T, Mimuro M, Fujita Y (1985) Estimation of phytoplankton photosynthesis using a fluorescence induction technique. J Plankton Res 7:679–689

    Article  CAS  Google Scholar 

  • Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol Oceanogr 49:1784–1793

    Article  CAS  Google Scholar 

  • Kainz M, Perga M-E, Arts MT, Mazumder A (2009) Essential fatty acid concentrations of different seston sizes and zooplankton: a field study of monomictic coastal lakes. J Plankton Res 31:635–645

    Article  CAS  Google Scholar 

  • Kolmakov VI, Gaevsky NA, Gold VM, Popelnitsky VA (2005) Estimation of primary production individual taxonomic groups of phytoplankton on the basis of a fluorescence method. Biol Inland Waters 4:13–18

    Google Scholar 

  • Lacroix G, Lescher-Moutoue F, Bertolo A (1999) Biomass and production of plankton in shallow and deep lakes: are there general patterns? Ann Limnol 35:111–122

    Article  Google Scholar 

  • Lands WEM (2009) Human life: caught in the food web. In: Arts MT, Kainz M, Brett MT (eds) Lipids in aquatic ecosystems. Springer, New York, pp 327–354

    Chapter  Google Scholar 

  • Lehninger AL, Nelson DL, Cox MM (1993) Principles of biochemistry, 2nd edn. Worth, New York

    Google Scholar 

  • Leonard AE, Pereira SL, Sprecher H, Huang Y-S (2004) Elongation of long-chain fatty acids. Prog Lipid Res 43:36–54

    Article  CAS  PubMed  Google Scholar 

  • Lindeman RL (1942) The trophic–dynamic aspect of ecology. Ecology 23:399–418

    Article  Google Scholar 

  • Maazouzi C, Masson G, Izquierdo MS, Pihan J-C (2008) Midsummer heat wave effects on lacustrine plankton: variation of assemblage structure and fatty acid composition. J Thermal Biol 33:287–296

    Article  CAS  Google Scholar 

  • Makhutova ON, Kalachova GS, Gladyshev MI (2003) A comparison of the fatty acid composition of Gammarus lacustris and its food sources from a freshwater reservoir, Bugach, and the saline Lake Shira in Siberia, Russia. Aquat Ecol 37:159–167

    Article  CAS  Google Scholar 

  • Muller-Navarra DC, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77

    Article  CAS  PubMed  Google Scholar 

  • Muller-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  PubMed  Google Scholar 

  • Oquist G, Hagstrom A, Alm P, Samuelsson G, Richardson K (1982) Chlorophyll a fluorescence, an alternative method for estimating primary production. Mar Biol 68:71–75

    Article  Google Scholar 

  • Pauly D, Christensen V (1995) Primary production required to sustain global fisheries. Nature 374:255–257

    Article  CAS  Google Scholar 

  • Plourde M, Cunnane SC (2007) Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl Physiol Nutr Metabol 32:619–634

    Article  CAS  Google Scholar 

  • Raffaelli D (2002) From Elton to mathematics and back again. Science 296:1035–1036

    Article  CAS  PubMed  Google Scholar 

  • Rao CRN (1984) Photosynthetically active components of global solar radiation: measurements and model computations. Meteorol Atmos Phys 34:353–364

    Google Scholar 

  • Rossi S, Sabates A, Latasa M, Reyes E (2006) Lipid biomarkers and trophic linkages between phytoplankton, zooplankton and anchovy (Engraulis encrasicolus) larvae in the NW Mediterranean. J Plankton Res 28:551–562

    Article  CAS  Google Scholar 

  • Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

    Article  CAS  Google Scholar 

  • Schulz M, Koschel R, Reese C, Mehner T (2004) Pelagic trophic transfer efficiency in an oligotrophic, dimictic deep lake (Lake Stechlin, Germany) and its relation to fisheries yield. Limnologica 34:264–273

    Google Scholar 

  • Smyntek PM, Teece MA, Schulz KL, Storch AJ (2008) Taxonomic differences in the essential fatty acid composition of groups of freshwater zooplankton relate to reproductive demands and generation time. Freshw Biol 53:1768–1782

    Article  CAS  Google Scholar 

  • Stockwell JD, Johannsson OE (1997) Temperature-dependent allometric models to estimate zooplankton production in temperate freshwater lakes. Can J Fish Aquat Sci 54:2350–2360

    Article  Google Scholar 

  • Sushchik NN, Gladyshev MI, Kalachova GS, Kravchuk ES, Dubovskaya OP, Ivanova EA (2003a) Particulate fatty acids in two small Siberian reservoirs dominated by different groups of phytoplankton. Freshw Biol 48:394–403

    Article  CAS  Google Scholar 

  • Sushchik NN, Gladyshev MI, Moskvichova AV, Makhutova ON, Kalachova GS (2003b) Comparison of fatty acid composition in major lipid classes of the dominant benthic invertebrates of the Yenisei River. Comp Biochem Phys B 134:111–122

    Article  CAS  Google Scholar 

  • Sushchik NN, Gladyshev MI, Makhutova ON, Kalachova GS, Kravchuk ES, Ivanova EA (2004) Associating particulate essential fatty acids of the ω-3 family with phytoplankton species composition in a Siberian reservoir. Freshw Biol 49:1206–1219

    Article  CAS  Google Scholar 

  • Taipale S, Kankaala P, Hamalainen H, Jones RI (2009) Seasonal shifts in the diet of lake zooplankton revealed by phospholipid fatty acid analysis. Freshw Biol 54:90–104

    Article  CAS  Google Scholar 

  • Tocher DR, Leaver MJ, Hodson PA (1998) Recent advances in the biochemistry and molecular biology of fatty acyl desaturase. Prog Lipid Res 37:73–117

    Article  CAS  PubMed  Google Scholar 

  • Vizcaino-Ochoa V, Lazo JP, Baron-Sevilla B, Drawbridge MA (2010) The effect of dietary docosahexaenoic acid (DHA) on growth, survival and pigmentation of California halibut Paralichthys californicus larvae (Ayres, 1810). Aquaculture 302:28–234

    Article  Google Scholar 

  • Wacker A, Von Elert E (2001) Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82:2507–2520

    Google Scholar 

Download references

Acknowledgments

The work was supported by “Thematic plans program” from the Ministry of Education and Sciences of Russian Federation (Theme B-4 of Siberian Federal University) and by a joint grant of the American Civilian Research and Development Foundation and the Ministry of Education and Sciences of Russian Federation (CRDF, project No. REC-002). We are grateful to handling editor, R.O.Hall, and two anonymous reviewers for their very helpful comments to improve the manuscript.

Author information

Authors and Affiliations

  1. Institute of Biophysics of Siberian Branch of Russian Academy of Sciences, Akademgorodok, Krasnoyarsk, 660036, Russia

    Michail I. Gladyshev, Nadezhda N. Sushchik, Olesia V. Anishchenko, Olesia N. Makhutova, Galina S. Kalachova, Anzhelika A. Kolmakova & Olga P. Dubovskaya

  2. Siberian Federal University, Svobodny av. 79, Krasnoyarsk, 660041, Russia

    Michail I. Gladyshev, Nadezhda N. Sushchik, Olesia V. Anishchenko, Olesia N. Makhutova, Vladimir I. Kolmakov, Galina S. Kalachova & Olga P. Dubovskaya

Authors
  1. Michail I. Gladyshev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nadezhda N. Sushchik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olesia V. Anishchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Olesia N. Makhutova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vladimir I. Kolmakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Galina S. Kalachova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anzhelika A. Kolmakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olga P. Dubovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michail I. Gladyshev.

Additional information

Communicated by Robert Hall.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gladyshev, M.I., Sushchik, N.N., Anishchenko, O.V. et al. Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir. Oecologia 165, 521–531 (2011). https://doi.org/10.1007/s00442-010-1843-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1843-6

Keywords

Search

Navigation