Skip to main content
SpringerLink
Log in

Transfer of Essential Substances from Phytoplankton to Zooplankton in Freshwater Ecosystems (Review)

  • Published:
Contemporary Problems of Ecology Aims and scope

Abstract

In freshwater ecosystems, the efficiency of transfer of essential substances from phytoplankton to zooplankton, measured as the ratio of the production of these substances in zooplankton to their production in phytoplankton, determines the functioning of higher trophic levels. In addition to carbon, primary producers transfer essential substances, including polyunsaturated fatty acids (PUFAs), nitrogen (N), and phosphorus (P), up the trophic chain. The transfer efficiency of these substances significantly varies in nature depending on environmental factors, which is reflected in the quality of biological resources. The purpose of this review is to analyze the mechanisms regulating the efficiency of the transfer of essential substances from phytoplankton to zooplankton and establish the main factors that may influence the efficiency of their transfer.

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

Similar content being viewed by others

REFERENCES

  1. Ahlgren, G., Goedkoop, W., Markensten, H., Sonesten, L., and Boberg, M., Seasonal variation in food quality for pelagic and benthic invertebrates in Lake Erken—the role of fatty acids, Freshwater Biol., 1997, vol. 38, no. 3, pp. 555–570. https://doi.org/10.1046/j.1365-2427.1997.00219.x

    Article  CAS  Google Scholar 

  2. Ahlgren, G., Gustafsson, I.-B., and Boberg, M., Fatty acid content and chemical composition of freshwater microalgae, J. Phycol., 1992, vol. 28, no. 1, pp. 37–50. https://doi.org/10.1111/j.0022-3646.1992.00037.x

    Article  CAS  Google Scholar 

  3. Andersen, T. and Hessen, D.O., Carbon, nitrogen, and phosphorus content of freshwater zooplankton, Limnol. Oceanogr., 1991, vol. 36, no. 4, pp. 807–814. https://doi.org/10.4319/lo.1991.36.4.0807

    Article  CAS  Google Scholar 

  4. Ballantyne, A.P., Brett, M.P., and Schindler, D.E., The importance of dietary phosphorus and highly unsaturated fatty acids for sockeye (Oncorhynchus nerka) growth in lake Washington—a bioenergetic approach, Can. J. Fish. Aquat. Sci., 2003, vol. 60, pp. 12–22. https://doi.org/10.1139/f02-166

    Article  CAS  Google Scholar 

  5. Bell, M.V. and Tocher, D.R., Biosynthesis of polyunsaturated fatty acids in aquatic ecosystems: general pathways and new directions, Lipids in Aquatic Ecosystems, New-York: Springer-Verlag, 2009, pp. 211–236.

    Google Scholar 

  6. Bell, M.V., Batty, R.S., Dick, J.R., Fretwell, K., Navarro, J.C., and Sargent, J.R., Dietary deficiency of docosahexaenoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus L.), Lipids, 1995, vol. 30, pp. 443–449.

    Article  CAS  Google Scholar 

  7. Bellou, S., Baeshen, M.N., Elazzazy, A.M., Aggeli, D., Sayegh, F., and Aggelis, G., Microalgal lipids biochemistry and biotechnological perspectives, Biotechnol. Adv., 2014, vol. 32, no. 8, pp. 1476–1493. https://doi.org/10.1016/j.biotechadv.2014.10.003

    Article  CAS  PubMed  Google Scholar 

  8. Beuckels, A., Smolders, E., and Muylaert, K., Nitrogen availability influences phosphorus removal in microalgae-based wastewater treatment, Water Res., 2015, vol. 77, pp. 98–106. https://doi.org/10.1016/j.watres.2015.03.018

    Article  CAS  PubMed  Google Scholar 

  9. Bohl, E., Food supply and prey selection in planktivorous cyprinidae, Oecologia, 1982, vol. 53, pp. 134–138.

    Article  Google Scholar 

  10. Brabrand, A., Faafeng, B., Källqvist, T., and Nilssen, P.J., Can iron defecation from fish influence phytoplankton production and biomass in eutrophic lakes?, Limnol. Oceanogr., 1984, vol. 29, no. 6, pp. 1330−1334. https://doi.org/10.4319/lo.1984.29.6.1330

    Article  CAS  Google Scholar 

  11. Brett, M.T. and Müller-Navarra, D.C., The role of highly unsaturated fatty acids in aquatic foodweb processes, Freshwater Biol., 1997, vol. 38, no. 3, pp. 483–500. https://doi.org/10.1046/j.1365-2427.1997.00220.x

    Article  CAS  Google Scholar 

  12. Brett, M.T., Müller-Navarra, D.C., and Persson, J., Crustacean zooplankton fatty acid composition, in Lipids in Aquatic Ecosystems, New-York: Springer-Verlag, 2009, pp. 115–146.

  13. Breuer, G., Evers, W.A.C., de Vree, J.H., Kleinegris, D.M.M., Martens, D.E., Wijffels, R.H., and Lamers, P.P., Analysis of fatty acid content and composition in microalgae, JoVE, 2013, vol. 80, art. ID e50628. https://doi.org/10.3791/50628

    Article  CAS  Google Scholar 

  14. Bulgakov, N.G. and Levich, A.P., Biogenic elements in the environment and phytoplankton: the ratio of nitrogen and phosphorus as an independent factor in regulating the structure of algocenosis, Usp. Sovrem. Biol., 1995, vol. 15, no. 1, pp. 13–23.

    Google Scholar 

  15. Burns, C.W., Brett, M.T., and Schallenberg, M.A., A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods, Freshwater Biol., 2011, vol. 56, no. 5, pp. 889–903. https://doi.org/10.1111/j.1365-2427.2010.02534.x

    Article  Google Scholar 

  16. Caramujo, M.-J., Boschker, H.T.S., and Admiraal, W., Fatty acid profiles of algae mark the development and composition of harpacticoid copepods, Freshwater Bio-l., 2008, vol. 53, no. 1, pp. 77–90. https://doi.org/10.1111/j.1365-2427.2007.01868.x

    Article  CAS  Google Scholar 

  17. Cloern, J.E., Why large cells dominate estuarine phytoplankton, Limnol. Oceanogr., 2018, vol. 63, no. S1, pp. S392–S409. https://doi.org/10.1002/lno.10749

    Article  Google Scholar 

  18. Conroy, J.D. and Culver, D.A., Do dreissenids mussels affect Lake Erie ecosystem stability processes?, Am. Midl. Nat., 2005, vol. 153, no. 1, pp. 20–32. https://doi.org/10.1674/0003-0031(2005)153[0020:DDMALE]2.0.CO;2

    Article  Google Scholar 

  19. Conroy, J.D., Kane, D.D., Dolan, D.M., Edwards, W.J., Charlton, M.N., and Culver, D.A., Temporal trends in Lake Erie plankton biomass: roles of external phosphorus loading and dreissenid mussels, J. Great Lakes Res., 2005, vol. 31, pp. 89–110. https://doi.org/10.1016/S0380-1330(05)70307-5

    Article  CAS  Google Scholar 

  20. Coppens, J., Decostere, B., Van Hulle, S., Nopens, I., Vlaeminck, S.E., De Gelder, L., and Boon, N., Kinetic exploration of nitrate-accumulating microalgae for nutrient recovery, Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 8377–8387.

    Article  CAS  Google Scholar 

  21. Dalsgaard, J., John, M.S., Kattner, G., Müller-Navarra, D., and Hagen, W., Fatty acid trophic markers in the pelagic marine environment, Adv. Mar. Biol., 2003, vol. 46, pp. 225–340. https://doi.org/10.1016/S0065-2881(03)46005-7

    Article  PubMed  Google Scholar 

  22. De Mott, W.R., The role of taste in food selection by freshwater zooplankton, Oecologia, 1986, vol. 69, pp. 334–340.

    Article  Google Scholar 

  23. Desvilettes, C., Bourdier, G., Amblard, C., and Barth, B., Use of fatty acids for the assessment of zooplankton grazing on bacteria, protozoans and microalgae, Freshwater Biol., 1997b, vol. 38, no. 3, pp. 629–637. https://doi.org/10.1046/j.1365-2427.1997.00241.x

    Article  CAS  Google Scholar 

  24. Desvilettes, C., Bourdier, G., and Breton, J.C., On the occurrence of a possible bioconversion of linolenic acid into docosahexaenoic acid by the copepod Eucyclops serrulatus fed on microalgae, J. Plankton Res., 1997a, vol. 19, no. 2, pp. 273–278. https://doi.org/10.1093/plankt/19.2.273

    Article  CAS  Google Scholar 

  25. Dijkman, N.A. and Kromkamp, J.C., Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition, Mar. Ecol.: Prog. Ser., 2006, vol. 324, pp. 113–125. https://doi.org/10.3354/meps324113

    Article  CAS  Google Scholar 

  26. Downing, J.A., Plante, C., and Lalonde, S., Fish production correlated with primary productivity, not the morphoedaphic Index, Can. J. Fish. Aquat. Sci., 1990, vol. 47, no. 8, pp. 1929–1936. https://doi.org/10.1139/f90-217

    Article  Google Scholar 

  27. Dubovskaya, O.P., Non-predatory mortality of the crustacean zooplankton, and its possible causes (a review), Zh. Obshch. Biol., 2009, vol. 70, no. 2, pp. 168–192.

    Google Scholar 

  28. Edwards, K.F., Klausmeier, C.A., and Litchman, E., Evidence for a three-way trade-off between nitrogen and phosphorus competitive abilities and cell size in phytoplankton, Ecology, 2011, vol. 92, no. 11, pp. 2085–2095. https://doi.org/10.1890/11-0395.1

    Article  PubMed  Google Scholar 

  29. Eixler, S., Karsten, U., and Selig, U., Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply, Phycologia, 2006, vol. 45, no. 1, pp. 53–60. https://doi.org/10.2216/04-79.1

    Article  Google Scholar 

  30. Elser, J.J., Dobberfuhl, D.R., MacKay, N.A., and Schampel, J.H., Organism size, life history, and N:P stoichiometry: Toward a unified view of cellular and ecosystem processes, Bioscience, 1996, vol. 46, no. 9, pp. 674–684. https://doi.org/10.2307/1312897

    Article  Google Scholar 

  31. Elser, J.J., O’Brien, W.J., Dobberfuhl, D.R., and Dowling, T.E., The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats, J. Evol. Biol., 2000, vol. 13, pp. 845–853.

    Article  Google Scholar 

  32. Feniova, I.Yu., Sakharova, E.G., Gladyshev,M.I., Sushchik, N.N., Gorelysheva, Z.I., and Karpowicz, M., Effects of fish on the transfer efficiency of carbon, PUFA and nutrients from phytoplankton to zooplankton under eutrophic conditions, Biol. Bull., 2021, vol. 48, no. 8, pp. 1284–1297. https://doi.org/10.1134/S1062359021080070

    Article  CAS  Google Scholar 

  33. Feniova, I., Dawidowicz, P., Ejsmont-Karabin, J., Gladyshev, M., Kalinowska, K., Karpowicz, M., Kostrzewska-Szlakowska, I., Majsak, N., Petrosyan, V., Razlutskij, V., Rzepecki, M., Sushchik, N., and Dzialowski, A.R., Effects of zebra mussels on cladoceran communities under eutrophic conditions, Hydrobiologia, 2018, vol. 822, pp. 37–54. https://doi.org/10.1007/s10750-018-3699-4

    Article  Google Scholar 

  34. Feniova, I., Dawidowicz, P., Gladyshev, M.I., Kostrzewska-Szlakowska, I., Rzepecki, M., Razlutskij, V., Sushchik, N.N., Majsak, N., and Dzialowski, A.R., Experimental effects of large-bodied Daphnia, fish and zebra mussels on cladoceran community and size structure, J. Plankton Res., 2015, vol. 37, no. 3, pp. 611–625. https://doi.org/10.1093/plankt/fbv022

    Article  CAS  Google Scholar 

  35. Feniova, I., Sakharova, E., Karpowicz, M., Gladyshev, M.I., Sushchik, N.N., Dawidowicz, P., Gorelysheva, Z., Górniak, A., Stroinov, Y., and Dzialowski, A., Direct and indirect impacts of fish on crustacean zooplankton in experimental mesocosms, Water, 2019, vol. 11, art. ID 2090. https://doi.org/10.3390/w11102090

    Article  CAS  Google Scholar 

  36. Feniova, I., Sakharova, E.G., Gorelysheva, Z.I., Karpowicz, M., Górniak, A., Petrosyan, V., and Dzialowski, A.R., Effects of zebra mussels (Dreissena polymorpha) on phytoplankton community structure under eutrophic conditions, Aquat. Invasions, 2020, vol. 15, no. 3, pp. 435–454. https://doi.org/10.3391/ai.2020.15.3.05

    Article  Google Scholar 

  37. Feniova, I.Y., Karpowicz, M., Gladyshev, M.I., Sushchik, N.N., Petrosyan, V.G., Sakharova, E.G., and Dzialowski, A.R., Effects of macrobiota on the transfer efficiency of essential elements and fatty acids from phytoplankton to zooplankton under eutrophic conditions, Front. Environ. Sci., 2021, vol. 9, art. ID 739014. https://doi.org/10.3389/fenvs.2021.739014

    Article  Google Scholar 

  38. Finkel, Z.V., Beardall, J., Flynn, K.J., Quigg, A., Rees, T.A.V., and Raven, J.A., Phytoplankton in a changing world: cell size and elemental stoichiometry, J. Plankton Res., 2010, vol. 32, no. 1, pp. 119–137. https://doi.org/10.1093/plankt/fbp098

    Article  CAS  Google Scholar 

  39. Frost, P.C., Evans-White, M.A., Finkel, Z.V., Jensen, T.C., and Matzek, V., Are you what you eat? Physiological constraints on organismal stoichiometry in an elementally imbalanced world, Oikos, 2005, vol. 109, no. 1, pp. 18–28. https://doi.org/10.1111/j.0030-1299.2005.14049.x

    Article  Google Scholar 

  40. Galloway, A.W.E. and Winder, M., Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids, PLoS One, 2015, vol. 10, no. 6 art. ID e0130053. https://doi.org/10.1371/journal.pone.0130053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Gladyshev, M.I., Essential polyunsaturated fatty acids and their dietary sources for man, Zh. Sib. Fed. Univ., 2012, vol. 5, no. 4, pp. 352–386.

    Article  Google Scholar 

  42. Gladyshev, M.I., Sushchik, N.N., Anishchenko, O.V., Makhutova, O.N., Kolmakov, V.I., Kalachova, G.S., Kolmakova, A.A., and Dubovskaya, O.P., Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir, Oecologia, 2011, vol. 165, pp. 521–531. https://doi.org/10.1007/s00442-010-1843-6

    Article  PubMed  Google Scholar 

  43. Gladyshev, M.I., Sushchik, N.N., Dubovskaya, O.P., Buseva, Z.F., Makhutova, O.N., Fefilova, E.N., Feniova, I.Y., Semenchenko, V.P., Kolmakova, A.A., and Kalachova, G.S., Fatty acid composition of Cladocera and Copepoda from lakes of contrasting temperature, Freshwater Biol., 2015, vol. 60, no. 2, pp. 373–386. https://doi.org/10.1111/fwb.12499

    Article  CAS  Google Scholar 

  44. Gladyshev, M.I., Sushchik, N.N., Kolmakova, A.A., Kalachova, G.S., Kravchuk, E.S., Ivanova, E.A., and Makhutova, O.N., Seasonal correlations of elemental and ω3 PUFA composition of seston and dominant phytoplankton species in a eutrophic Siberian Reservoir, Aquat. Ecol., 2007, vol. 41, pp. 9–23. https://doi.org/10.1007/s10452-006-9040-8

    Article  CAS  Google Scholar 

  45. Gladyshev, M.I., Temerova, T.A., Dubovskaya, O.P., Kolmakov, V.I., and Ivanova, E.A., Selective grazing on Cryptomonas by Ceriodaphnia quadrangula fed a natural phytoplankton assemblage, Aquat. Ecol., 1999, vol. 33, pp. 347–353.

    Article  Google Scholar 

  46. Gliwicz, Z.M., Between hazards of starvation and risk of predation: the ecology of off-shore animals, Excellence in Ecology, Germany: Oldendorf/Luhe, 2003.

    Google Scholar 

  47. Gugger, M., Lyra, C., Suominen, I., Tsitko, I., Humbert, J.-F., Salkinoja-Salonen, M.S., and Sivonen, K., Cellular fatty acids as chemotaxonomic markers of the genera Anabaena, Aphanizomenon, Microcystis, Nostoc and Planktothrix (cyanobacteria), Int. J. Syst. Evol. Microbiol., 2002, vol. 52, no. 3, pp. 1007–1015. https://doi.org/10.1099/00207713-52-3-1007

    Article  CAS  PubMed  Google Scholar 

  48. Guschina, I.A. and Harwood, J.L., Mechanisms of temperature adaptation in poikilotherms, FEBS Lett., 2006, vol. 580, no. 23, pp. 5477–5483. https://doi.org/10.1016/j.febslet.2006.06.066

    Article  CAS  PubMed  Google Scholar 

  49. Gutseit, K., Berglund, O., and Granéli, W., Essential fatty acids and phosphorus in seston from lakes with contrasting terrestrial dissolved organic carbon content, Freshwater Biol., 2007, vol. 52, no. 1, pp. 28–38. https://doi.org/10.1111/j.1365-2427.2006.01668.x

    Article  CAS  Google Scholar 

  50. Happey-Wood, C.M. and Pentecost, A., Algal bioassay of the water from two linked but contrasting Welsh lakes, Freshwater Biol., 1981, vol. 11, no. 5, pp. 473–491. https://doi.org/10.1111/j.1365-2427.1981.tb01278.x

    Article  CAS  Google Scholar 

  51. Heckmann, L.-H., Sibly, R.M., Timmermans, M.JTN., and Callaghan, A., Outlining eicosanoid biosynthesis in the crustacean Daphnia, Front. Zool., 2008, vol. 5, art. ID 11. https://doi.org/10.1186/1742-9994-5-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Hessen, D.O. and Leu, E., Trophic transfer and trophic modification of fatty acids in high Arctic lakes, Freshwater Biol., 2006, vol. 51, no. 11, pp. 1987–1998. https://doi.org/10.1111/j.1365-2427.2006.01619.x

    Article  CAS  Google Scholar 

  53. Hessen, D.O., Carbon, nitrogen and phosphorus status in Daphnia at varying food conditions, J. Plankton Res., 1990, vol. 12, no. 6, pp. 1239–1249. https://doi.org/10.1093/plankt/12.6.1239

    Article  CAS  Google Scholar 

  54. Hessen, D.O., Elser, J.J., Sterner, R.W., Urabe J. Ecological stoichiometry: an elementary approach using basic principles, Limnol. Oceanogr., 2013, vol. 58, no. 6, pp. 2219–2236. https://doi.org/10.4319/lo.2013.58.6.2219

    Article  CAS  Google Scholar 

  55. Hessen, D.O., Nutrient element limitation of zooplankton production, Am. Nat., 1992, vol. 140, no. 5, pp. 799–814.

    Article  Google Scholar 

  56. Hixson, S.M. and Arts, M.T., Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton, Global Change Biol., 2016, vol. 22, no. 8, pp. 2744–2755. https://doi.org/10.1111/gcb.13295

    Article  Google Scholar 

  57. Iwabuchi, T. and Urabe, J., Phosphorus acquisition and competitive abilities of two herbivorous zooplankton, Daphnia pulex and Ceriodaphnia quadrangular, Ecol. Res., 2010, vol. 25, no. 3, pp. 619–627.

    Article  Google Scholar 

  58. Izquierdo, M.S., Fernandez-Palacios, H., and Tacon, A.G.J., Effect of broodstock nutrition on reproductive performance of fish, Aquaculture, 2001, vol. 197, no. 1–4, pp. 25–42. https://doi.org/10.1016/S0044-8486(01)00581-6

    Article  Google Scholar 

  59. Jardine, T.D., Galloway, A.W.E., and Kainz, M.J., U-nlocking the power of fatty acids as dietary tracers and metabolic signals in fishes and aquatic invertebrates, Philos. Trans. R. Soc., 2020, vol. 375, no. 1804, art. ID 20190639. https://doi.org/10.1098/rstb.2019.0639

  60. Kainz, M., Arts, M.T., and Mazumder, A., Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels, Limnol. Oceanogr., 2004, vol. 49, no. 5, pp. 1784–1793. https://doi.org/10.4319/lo.2004.49.5.1784

    Article  CAS  Google Scholar 

  61. Karpowicz, M., Feniova, I., Gladyshev, M.I., Ejsmont-Karabin, J., Górniak, A., Zieliński, P., Dawidowicz, P., Kolmakova, A.A., and Dzialowski, A.R., The stoichiometric ratios (C:N:P) in a pelagic food web under experimental conditions, Limnologica, 2019, vol. 77, art. ID 125690. https://doi.org/10.1016/j.limno.2019.125690

    Article  CAS  Google Scholar 

  62. Kelly, J.R. and Scheibling, R.E., Fatty acids as dietary tracers in benthic food webs, Mar. Ecol.: Prog. Ser., 2012, vol. 446, pp. 1–22. https://doi.org/10.3354/meps09559

    Article  CAS  Google Scholar 

  63. Klausmeier, C.A., Litchman, E., Daufresne, T., and Levin, S.A., Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Nature, 2004, vol. 429, no. 6988, pp. 171–174.

    Article  CAS  Google Scholar 

  64. Knoll, L.B., Sarnelle, O., Hamilton, S.K., Kissman, C.E.H., Wilson, A.E., Rose, J.B., and Morgan, M.R., Invasive zebra mussels (Dreissena polymorpha) increase cyanobacterial toxin concentrations in low-nutrient lakes, Can. J. Fish Aquat. Sci., 2008, vol. 65, pp. 448–455. https://doi.org/10.1139/f07-181

    Article  CAS  Google Scholar 

  65. Kormilets, O.N., Fatty acids in food webs of inland water ecosystems, Doctoral (Biol.) Dissertation, Krasnoyarsk, 2019.

  66. Lacroix, G., Lescher-Moutoue, F., and Bertolo, A., Biomass and production of plankton in shallow and deep lakes: are there general patterns?, Ann. Limnol., 1999, vol. 35, no. 2, pp. 111–122. https://doi.org/10.1051/limn/1999016

    Article  Google Scholar 

  67. Leonard, A.E., Pereira, S.L., Sprecher, H., and Huang, Y-S., Elongation of long-chain fatty acids, Prog. Lipid Res., 2004, vol. 43, pp. 36–54. https://doi.org/10.1016/s0163-7827(03)00040-7

    Article  CAS  PubMed  Google Scholar 

  68. Levich, A.P. and Bulgakov, N.G., Regulation of species and size composition in phytoplankton communities in situ by N:P ratio, Russ. J. Aquat. Ecol., 1992, vol. 2, pp. 149–159.

    Google Scholar 

  69. Lin, C.K. and Schelske, C.L., Seasonal variation of potential nutrient limitation to chlorophyll production in southern Lake Huron, Can. J. Fish Aquat. Sci., 1981, vol. 38, pp. 1–9. https://doi.org/10.1139/f81-001

    Article  Google Scholar 

  70. Lindeman, R.L., The trophic–dynamic aspect of ecology, Ecology, 1942, vol. 23, no. 4, pp. 399–418.

    Article  Google Scholar 

  71. Loladze, I. and Elser, J.J., The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio, Ecol. Lett., 2011, vol. 14, no. 3, pp. 244–250. https://doi.org/10.1111/j.1461-0248.2010.01577.x

    Article  PubMed  Google Scholar 

  72. Makhutova, O.N., Protasov, A.A., Gladyshev, M., Sylaieva, A.A., Sushchik, N.N., Morozovskaya, I.A, and Kalachova, G.S., Feeding spectra of bivalve mollusks Unio and Dreissena from Kanevskoe Reservoir, Ukraine: are they food competitors or not?, Zool. Stud., 2013, vol. 52, no. 56, art. ID 56.

    Article  Google Scholar 

  73. Martin-Creuzburg, D., Wacker, A., and Basena, T., Interactions between limiting nutrients: Consequences for somatic and population growth of Daphnia magna, Limnol. Oceanogr., 2010, vol. 55, no. 6, pp. 2597–2607. https://doi.org/10.4319/lo.2010.55.6.2597

    Article  CAS  Google Scholar 

  74. Müller-Navarra, D.C., Brett, M.T., Liston, A.M., and Goldman, C.R., A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers, Nature, 2000, vol. 403, pp. 74–77.

    Article  Google Scholar 

  75. Müller-Navarra, D.C., Brett, M.T., Park, S., Chandra, S., Ballantyne, A.P., Zorita, E., and Goldman, C.R., Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes, Nature, 2004, vol. 427, pp. 69–72.

    Article  Google Scholar 

  76. Okun, N. and Mehner, T., Distribution and feeding of juvenile fish on invertebrates in littoral reed (Phragmites) stands, Ecol. Freshwater Fish, 2005, vol. 14, no. 2, pp. 139–149. https://doi.org/10.1111/j.1600-0633.2005.00087.x

    Article  Google Scholar 

  77. Olsen, Y., Jensen, A., Reinertsen, H., Børsheim, K.Y., Heldal, M., and Langeland, A., Dependence of the rate of release of phosphorus by zooplankton on the P:C ratio in the food supply, as calculated by a recycling model, Limnol. Oceanogr., 1986, vol. 31, no. 1, pp. 34–44. https://doi.org/10.4319/lo.1986.31.1.0034

    Article  Google Scholar 

  78. Parrish, C.C., Whiticar, M., and Puvanendran, V., Is ω6 docosapentaenoic acid an essential fatty acid during early ontogeny in marine fauna?, Limnol. Oceanogr., 2007, vol. 52, no. 1, pp. 476–479. https://doi.org/10.4319/lo.2007.52.1.0476

    Article  CAS  Google Scholar 

  79. Persson, J., Brett, M.T., Vrede, T., and Ravet, J.L., Food quantity and quality regulation of trophic transfer between primary producers and a keystone grazer (Daphnia) in pelagic freshwater food webs, Oikos, 2007, vol. 116, no. 7, pp. 1152–1163. https://doi.org/10.1111/j.0030-1299.2007.15639.x

    Article  Google Scholar 

  80. Powell, N., Shilton, A., Chisti, Y., and Pratt, S., Towards a luxury uptake process via microalgae—Defining the polyphosphate dynamics, Water Res., 2009, vol. 43, no. 17, pp. 4207–4213. https://doi.org/10.1016/j.watres.2009.06.011

    Article  CAS  PubMed  Google Scholar 

  81. Prater, C., Wagner, N.D., and Frost, P.C., Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations, Limnol. Oceanogr., 2018, vol. 63, no. 4, pp. 1727–1740. https://doi.org/10.1002/lno.10803

    Article  CAS  Google Scholar 

  82. Raikow, D.F., Sarnelle, O., Wilson, A.E., and Hamilton, S.K., Dominance of the noxious cyanobacterium Microcystis aeruginosa in low-nutrient lakes is associated with exotic zebra mussels, Limnol. Oceanogr., 2004, vol. 49, no. 2, pp. 482–487. https://doi.org/10.4319/lo.2004.49.2.0482

    Article  Google Scholar 

  83. Ravet, J.L., Brett, M.T., and Arhonditsis, G.B., The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA, Ecology, 2010, vol. 91, no. 1, pp. 180–190. https://doi.org/10.1890/08-2037.1

    Article  PubMed  Google Scholar 

  84. Redfield, A.C., On the proportions of organic derivatives in sea water and their relation to the composition of plankton, James Johnstone Memorial Volume, Liverpool: University Press of Liverpool, 1934, pp. 176–192.

    Google Scholar 

  85. Reynolds, C., Ecology of Phytoplankton, Cambridge: Cambridge University Press, 2006.

    Book  Google Scholar 

  86. Sakharova, E.G., Karpowicz, M., Gladyshev, M.I., Sushchik, N.N., Gorelysheva, Z.I., and Feniova, I.Yu., Effects of Dreissena polymorpha on the transfer efficiency of carbon, fatty acids, nitrogen, and phosphorus from phytoplankton to zooplankton, Zh. Obshch. Biol., 2021, vol. 82, no. 3, pp. 188–200. https://doi.org/10.31857/S0044459621030052

    Article  Google Scholar 

  87. Sargent, J., Bell, G., McEvoy, L., Tocher, D., and Estevez, A., Recent developments in the essential fatty acid nutrition of fish, Aquaculture, 1999, vol. 177, nos. 1–4, pp. 191–199. https://doi.org/10.1016/S0044-8486(99)00083-6

    Article  CAS  Google Scholar 

  88. Sarnelle, O., White, J.D., Horst, G.P., and Hamilton, S.K., Phosphorus addition reverses the positive effect of zebra mussels (Dreissena polymorpha) on the toxic cyanobacterium, Microcystis aeruginosa, Water Res., 2012, vol. 46, no. 11, pp. 3471–3478. https://doi.org/10.1016/j.watres.2012.03.050

    Article  CAS  PubMed  Google Scholar 

  89. Schmitz, G. and Ecker, J., The opposing effects of n-3 and n-6 fatty acids, Prog. Lipid Res., 2008. vol. 47, no. 2, pp. 147–155. https://doi.org/10.1016/j.plipres.2007.12.004

    Article  CAS  PubMed  Google Scholar 

  90. Schulhof, M.A., Shurin, J.B., and Declerck, S.A.J., Van de Waal D.B. Phytoplankton growth and stoichiometric responses to warming, nutrient addition and grazing depend on lake productivity and cell size, Global Change Biol., 2019, vol. 25, no. 8, pp. 2751–2762. https://doi.org/10.1111/gcb.14660

    Article  Google Scholar 

  91. Sommer, U. and Sommer, F., Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton, Oecologia, 2006, vol. 147, pp. 183–194.

    Article  Google Scholar 

  92. Sperfeld, E. and Wacker, A., Temperature- and cholesterol induced changes in eicosapentaenoic acid limitation of Daphnia magna determined by a promising method to estimate growth saturation thresholds, Limnol. Oceanogr., 2011, vol. 56, no. 4, pp. 1273–1284. https://doi.org/10.4319/lo.2011.56.4.1273

    Article  CAS  Google Scholar 

  93. Sterner, R.W. and Elser, J.J., Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere, Oxford: Princeton Univ. Press, 2002.

    Google Scholar 

  94. Sterner, R.W. and Hessen, D.O., Algal nutrient limitation and the nutrition of aquatic herbivores, Annu. Rev. Ecol. Syst., 1994, vol. 25, pp. 1–29. https://doi.org/10.1146/annurev.es.25.110194.000245

    Article  Google Scholar 

  95. Sterner, R.W., Daphnia growth on varying quality of Scenedesmus: mineral limitation of zooplankton, Ecology, 1993, vol. 74, no. 8, pp. 2351–2360. https://doi.org/10.2307/1939587

    Article  Google Scholar 

  96. Sterner, R.W., Modelling interactions of food quality and quantity in homeostatic consumers, Freshwater Biol., 1997, vol. 38, no. 3, pp. 473–481. https://doi.org/10.1046/j.1365-2427.1997.00234.x

    Article  Google Scholar 

  97. Sterner, R.W., The ratio of nitrogen to phosphorus resupplied by herbivores: Zooplankton and the algal competitive arena, Am. Nat., 1990, vol. 136, no. 2, pp. 209–229.

    Article  Google Scholar 

  98. Sterner, R.W., The role of grazers in phytoplankton succession, Plankton Ecology, Brock: Springer-Verlag, 1989, pp. 107–170.

    Google Scholar 

  99. Strandberg, U., Taipale, S.J., Hiltunen, M., Galloway, A.W.E., Brett, M.T., and Kankaala, P., Inferring phytoplankton community composition with a fatty acid mixing model, Ecosphere, 2015, vol. 6, no. 1, pp. 1–14. https://doi.org/10.1890/ES14-00382.1

    Article  Google Scholar 

  100. Sushchik, N.N., Gladyshev, M.I., Makhutova, O.N., Kalachova, G.S., Kravchuk, E.S., and Ivanova, E.A., Associating particulate essential fatty acids of the ω3 family with phytoplankton species composition in a Siberian reservoir, Freshwater Biol., 2004, vol. 49, no. 9, pp. 1206–1219. https://doi.org/10.1111/j.1365-2427.2004.01263.x

    Article  CAS  Google Scholar 

  101. Sushchik, N.N., Kalachova, G.S., Zhila, O.N., Gladyshev, M.I., and Volova, T.G., A temperature dependence of the intra- and extracellular fatty acid composition of green algae and cyanobacterium, Russ. J. Plant Physiol., 2003, vol. 50, pp. 374–380.

    Article  CAS  Google Scholar 

  102. Taipale, S., Strandberg, U., Peltomaa, E., Galloway, A.W.E., Ojala, A., and Brett, M.T., Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes, Aquat. Microb. Ecol., 2013, vol. 71, no. 2, pp. 165–178. https://doi.org/10.3354/ame01671

    Article  Google Scholar 

  103. Taipale, S.J., Kainz, M.J., and Brett, M.T., Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia, Oikos, 2011, vol. 120, no. 11, pp. 1674–1682. https://doi.org/10.1111/j.1600-0706.2011.19415.x

    Article  Google Scholar 

  104. Taipale, S.J., Vuorio, K., Brett, M.T., Peltomaa, E., Hiltunen, M., and Kankaala, P., Lake zooplankton delta C-13 values are strongly correlated with the delta C-13 values of distinct phytoplankton taxa, Ecosphere, 2016, vol. 7, no. 8, art. ID e01392. https://doi.org/10.1002/ecs2.1392

    Article  Google Scholar 

  105. Tocher, D.R., Leaver, M.J., and Hodson, P.A., Recent advances in the biochemistry and molecular biology of fatty acyl desaturase, Prog. Lipid Res., 1998, vol. 37, pp. 73–117. https://doi.org/10.1016/s0163-7827(98)00005-8

    Article  CAS  PubMed  Google Scholar 

  106. Toseland, A., Daines, S.J., Clark, J.R., Kirkham, A., Strauss, J., Uhlig, C., and Mock, T., The impact of temperature on marine phytoplankton resource allocation and metabolism, Nat. Clim. Change, 2013, vol. 3, no. 11, pp. 979–984.

    Article  CAS  Google Scholar 

  107. Twining, C.W., Brenna, J.T., Hairston, N.G., and Flecker, A.S., Highly unsaturated fatty acids in nature: What we know and what we need to learn, Oikos, 2016, vol. 125, no. 6, pp. 749–760. https://doi.org/10.1111/oik.02910

    Article  CAS  Google Scholar 

  108. Urabe, J. and Watanabe, Y., Possibility of N or P limitation for planktonic cladocerans: An experimental test, Limnol. Oceanogr., 1992, vol. 37, no. 2, pp. 244–251. https://doi.org/10.4319/lo.1992.37.2.0244

    Article  CAS  Google Scholar 

  109. Vanderploeg, H.A., Sarnelle, O., Liebig, J.R., Morehead, N.R., Robinson, S.D., Johengen, T.H., and Horst, G.P., Seston quality drives feeding, stoichiometry and excretion of zebra mussels, Freshwater Biol., 2017, vol. 62, no. 4, pp. 664–680. https://doi.org/10.1111/fwb.12892

    Article  CAS  Google Scholar 

  110. Vanni, M.J., Nutrient cycling by animals in freshwater ecosystems, Annu. Rev. Ecol. Syst., 2002, vol. 33, pp. 341–370. https://doi.org/10.1146/annurev.ecolsys.33.010802.150519

    Article  Google Scholar 

  111. Velthuis, M., De Senerpont Domis, L.N., Frenken, T., Stephan, S., Kazanjian, G., Aben, R., Kosten, S., Van Donk, E., and Van De Waal, D.B., Warming advances top-down control and reduces producer biomass in a freshwater plankton community, Ecosphere, 2017, vol. 8, no. 1, pp. 1–16. https://doi.org/10.1002/ecs2.1651

    Article  Google Scholar 

  112. Waajen, G.W.A.M., Van Bruggen, N.C.B., Pires, L.M.D., Lengkeek, W., and Lürling, M., Biomanipulation with quagga mussels (Dreissena rostriformis bugensis) to control harmful algal blooms in eutrophic urban ponds, Ecol. Eng., 2016, vol. 90, pp. 141–150. https://doi.org/10.1016/j.ecoleng.2016.01.036

    Article  Google Scholar 

  113. Wagner, N.D., Hillebrand, H., Wacker, A., and Frost, P.C., Nutritional indicators and their uses in ecology, Ecol. Lett., 2013, vol. 16, no. 4, pp. 535–544. https://doi.org/10.1111/ele.12067

    Article  PubMed  Google Scholar 

  114. Wagner, N.D., Lankadurai, B.P., Simpson, M.J., Simpson, A.J., and Frost, P.C., Metabolomic differentiation of nutritional stress in an aquatic invertebrate, Physiol. Biochem. Zool., 2015, vol. 88, no. 1, pp. 43–52. https://doi.org/10.1086/679637

    Article  PubMed  Google Scholar 

  115. Weers, P.M.M., Siewertsen, K., and Gulati, R., Is the fatty acid composition of Daphnia galeata determined by the fatty acid composition of the ingested diet?, Freshwater Biol., 1997, vol. 38, no. 3, pp. 731–738. https://doi.org/10.1046/j.1365-2427.1997.00238.x

    Article  CAS  Google Scholar 

  116. White, T.C.R., The Inadequate Environment: Nitrogen and the Abundance of Animals, Berlin: Springer-Verlag, 1993.

    Book  Google Scholar 

Download references

Funding

The analysis and interpretation of the literature on zooplankton were supported by the Russian Science Foundation, project no. 21-14-00123, and the literature on phytoplankton was analyzed and interpreted as part of State Task topic no. 121051100099-5. The preparation of the manuscript by Feniova I. was supported by the Polish National Agency for Academic Exchange (Agreement No. PPN/ULM/2020/ 1/00258/U/DRAFT/00001).

Author information

Authors and Affiliations

  1. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    I. Yu. Feniova

  2. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Russia

    E. G. Sakharova & A. V. Krylov

Authors
  1. I. Yu. Feniova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. G. Sakharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. V. Krylov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. G. Sakharova.

Ethics declarations

The authors declare that they have no conflict of interests.

Additional information

Translated by D. Zabolotny

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feniova, I.Y., Sakharova, E.G. & Krylov, A.V. Transfer of Essential Substances from Phytoplankton to Zooplankton in Freshwater Ecosystems (Review). Contemp. Probl. Ecol. 15, 315–326 (2022). https://doi.org/10.1134/S1995425522040059

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1995425522040059

Keywords:

Search

Navigation