Ecological significance of sterols in aquatic food webs



Sterols are indispensable for a multitude of physiological processes in all eukaryotic organisms. In most eukaryotes, sterols are synthesized de novo from low molecular weight precursors. Some invertebrates (e.g., all arthropods examined to date), however, are incapable of synthesizing sterols de novo, and therefore have to acquire sterols from their diet. Here, we aim to demonstrate that such nutritional requirements not only affect the performance of an individual in its environment but may also have major consequences for the function of aquatic ecosystems. Starting from general patterns of occurrence and biosynthesis of sterols, we next explore the physiological properties and nutritional requirements of sterols. These aspects are then integrated into a more ecological perspective. We emphasize their effects on aquatic food webs in general and on herbivorous zooplankton in particular with the major aim to outline how the interplay of physiological capabilities of individual herbivores and trophic interactions in the food web will determine the effect of low dietary provision of sterols on structure and function of aquatic ecosystems.


Sterol Content Sterol Composition Herbivorous Zooplankton Heterotrophic Protist Dietary Sterol 
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.


  1. Ballantine, J.A., Lavis, A., and Morris, R.J. 1979. Sterols of the phytoplankton – effects of illumination and growth stage. Phytochemistry 18:1459–1466.CrossRefGoogle Scholar
  2. Barrett, S.M., Volkman, J.K., Dunstan, G.A., and Leroi, J.M. 1995. Sterols of 14 species of marine diatoms (bacillariophyta). J. Phycol. 31:360–369.CrossRefGoogle Scholar
  3. Bec, A., Martin-Creuzburg, D., and Von Elert, E. 2006. Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnol. Oceanogr. 51:1699–1707.CrossRefGoogle Scholar
  4. Behmer, S.T., and Elias, D.O. 1999. The nutritional significance of sterol metabolic constraints in the generalist grasshopper Schistocerca americana. J. Insect Physiol. 45:339–348.PubMedCrossRefGoogle Scholar
  5. Behmer, S.T., and Elias, D.O. 2000. Sterol metabolic constraints as a factor contributing to the maintenance of diet mixing in grasshoppers (Orthoptera:Acrididae). Physiol. Biochem. Zool. 73:219–230.PubMedCrossRefGoogle Scholar
  6. Behmer, S.T., and Nes, W.D. 2003. Insect sterol nutrition and physiology: a global overview. Adv. Insect Physiol. 31:1–72.CrossRefGoogle Scholar
  7. Behmer, S.T., Elias, D.O., and Bernays, E.A. 1999a. Post-ingestive feedbacks and associative learning regulate the intake of unsuitable sterols in a generalist grasshopper. J. Exp. Biol. 202:739–748.Google Scholar
  8. Behmer, S.T., Elias, D.O., and Grebenok, R.J. 1999b. Phytosterol metabolism and absorption in the generalist grasshopper, Schistocerca americana (Orthoptera: Acrididae). Arch. Insect Biochem. Physiol. 42:13–25.CrossRefGoogle Scholar
  9. Boëchat, I.G., and Adrian, R. 2006. Evidence for biochemical limitation of population growth and reproduction of the rotifer Keratella quadrata fed with freshwater protists. J. Plankton Res. 28:1027–1038.CrossRefGoogle Scholar
  10. Boëchat, I.G., Krüger, A., and Adrian, R. 2007. Sterol composition of freshwater algivorous ciliates does not resemble dietary composition. Microb. Ecol. 53:74–81.PubMedCrossRefGoogle Scholar
  11. Champagne, D.E., and Bernays, E.A. 1991. Phytosterol unsuitability as a factor mediating food aversion learning in the grasshopper Schistocerca americana. Physiol. Entomol. 16:391–400.CrossRefGoogle Scholar
  12. Conklin, D.E., and Provasoli, L. 1977. Nutritional requirements of the water flea Moina macrocopa. Biol. Bull. 152:337–350.CrossRefGoogle Scholar
  13. Conner, R.L., Landrey, J.R., Burns, C.H., and Mallory, F.B. 1968. Cholesterol inhibition of pentacyclic triterpenoid biosynthesis in Tetrahymena pyriformis. J. Protozool. 15:600–605.PubMedGoogle Scholar
  14. Crockett, E.L., and Hassett, R.P. 2005. A cholesterol-enriched diet enhances egg production and egg viability without altering cholesterol content of biological membranes in the copepod Acartia hudsonica. Physiol. Biochem. Zool. 78:424–433.PubMedCrossRefGoogle Scholar
  15. Dahl, C.E., Dahl, J.S., and Bloch, K. 1980. Effect of alkyl-substituted precursors of cholesterol on artificial and natural membranes and on the viability of Mycoplasma capricolum. Biochemistry 19:1462–1467.PubMedCrossRefGoogle Scholar
  16. Dembitsky, V.M., Rezanka, T., and Srebnik, M. 2003. Lipid compounds of freshwater sponges: family Spongillidae, class Demospongiae. Chem. Phys. Lipids 123:117–155.PubMedCrossRefGoogle Scholar
  17. Ederington, M., McManus, G.B., and Harvey, H.R. 1995. Trophic transfer of fatty acids, sterols, and a triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol. Oceanogr. 40:860–867.CrossRefGoogle Scholar
  18. Frolov, A.V., Pankov, S.L., Geradz, K.N., Pankova, S.A., and Spektrova, L.V. 1991. Influence of the biochemical composition of food on the biochemical composition of the rotifer Brachionus plicatilis. Aquaculture 97:181–202.CrossRefGoogle Scholar
  19. Gessner, M.O., and Chauvet, E. 1993. Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl. Environ. Microb. 59:502–507.Google Scholar
  20. Gilbert, L.I., Rybczynski, R., and Warren, J.T. 2002. Control and biochemical nature of the ecdysteroidogenic pathway. Annu. Rev. Entomol. 47:883–916.PubMedCrossRefGoogle Scholar
  21. Giner, J.-L., Faraldos, J.A., and Boyer, G.L. 2003. Novel sterols of the toxic dinoflagellate Karenia brevis (Dinophyceae): a defensive function for unusual marine sterols? J. Phycol. 39:315–319.CrossRefGoogle Scholar
  22. Goad, L.J. 1981. Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl. Chem. 51:837–852.CrossRefGoogle Scholar
  23. Grieneisen, M.L. 1994. Recent advances in our knowledge of ecdysteroid biosynthesis in insects and crustaceans. Insect Biochem. Mol. Biol. 24:115–132.CrossRefGoogle Scholar
  24. Guisande, C., Riverio, I., and Maneiro, I. 2000. Comparisons among the amino acid composition of females, eggs and food to determine the relative importance of the food quantity and food quality to copepod reproduction. Mar. Ecol. Prog. Ser. 202:135–142.CrossRefGoogle Scholar
  25. Haines, T.H. 2001. Do sterols reduce proton and sodium leaks through lipid bilayers? Prog. Lipid Res. 40:299–324.CrossRefGoogle Scholar
  26. Harvey, H.R., and McManus, G.B. 1991. Marine ciliates as a widespread source of tetrahymanol and hopan-3β-ol in sediments. Geochim. Cosmochim. Acta 55:3387–3390.CrossRefGoogle Scholar
  27. Harvey, H.R., Eglinton, G., O’Hara, S.C.M., and Corner, E.D.S. 1987. Biotransformation and assimilation of dietary lipids by Calanus feeding on a dinoflagellate. Geochim. Cosmochim. Acta 51:3031–3040.CrossRefGoogle Scholar
  28. Harvey, H.R., O’Hara, S.C.M., Eglinton, G., and Corner, E.D.S. 1989. The comparative fate of dinosterol and cholesterol in copepod feeding: implications for a conservative molecular biomarker in the marine water column. Org. Geochem. 14:635–641.CrossRefGoogle Scholar
  29. Harvey, H.R., Ederington, M.C., and McManus, G.B. 1997. Lipid composition of the marine ciliates Pleuronema sp. and Fabrea salina: shifts in response to changes in diets. J. Eukaryot. Microbiol. 44:189–193.Google Scholar
  30. Hassett, R.P. 2004. Supplementation of a diatom diet with cholesterol can enhance copepod egg-production rates. Limnol. Oceanogr. 49:488–494.CrossRefGoogle Scholar
  31. Kanazawa, A. 2001. Sterols in marine invertebrates. Fish. Sci. 67:997–1007.CrossRefGoogle Scholar
  32. Klein Breteler, W.C.M., Schogt, N., Baas, M., Schouten, S., and Kraay, G.W. 1999. Trophic upgrading of food quality by protozoans enhancing copepod growth: the role of essential lipids. Mar. Biol. 135:191–198.CrossRefGoogle Scholar
  33. Klein Breteler, W.C.M., Koski, M., and Rampen, S. 2004. Role of essential lipids in copepod nutrition: no evidence for trophic upgrading of food quality by a marine ciliate. Mar. Ecol. Prog. Ser. 274:199–208.CrossRefGoogle Scholar
  34. Klein Breteler, W.C.M., Schogt, N., and Rampen, S. 2005. Effect of diatom nutrient limitation on copepod development: role of essential lipids. Mar. Ecol. Prog. Ser. 291:125–133.CrossRefGoogle Scholar
  35. Lampert, W., and Trubetskova, I. 1996. Juvenile growth rate as a measure of fitness in Daphnia. Funct. Ecol. 10:631–635.CrossRefGoogle Scholar
  36. Leblond, J.D., and Chapman, P.J. 2002. A survey of the sterol composition of the marine dinoflagellates Karenia brevis, Karenia mikimotoi, and Karlodinium micrum: distribution of sterols within other members of the class dinophyceae. J. Phycol. 38:670–682.CrossRefGoogle Scholar
  37. Leppimäki, P, Mattinen, J., and Slotte, P. 2000. Sterol-induced upregulation of phosphatidylcholine synthesis in cultured fibroblasts is affected by the double-bond position in the sterol tetracyclic ring structure. Eur. J. Biochem. 267:6385–6394.PubMedCrossRefGoogle Scholar
  38. Lozano, R., Salt, T.A., Chitwood, D.J., Lusby, W.R., and Thompson, M.J. 1987. Metabolism of sterols of varying ring unsaturation and methylation by Caenorhabditis elegans. Lipids 22:84–87.PubMedCrossRefGoogle Scholar
  39. Lynch, M., Weider, L.J., and Lampert, W. 1986. Measurement of the carbon balance in Daphnia. Limnol. Oceanogr. 31:17–33.CrossRefGoogle Scholar
  40. MacLatchy, D.L., and Van der Kraak, G. 1995. The phytoestrogen β-sitosterol alters the reproductive endocrine status of goldfish. Toxicol. Appl. Pharmacol. 134:305–312.PubMedCrossRefGoogle Scholar
  41. Martin-Creuzburg, D., and Von Elert, E. 2004. Impact of 10 dietary sterols on growth and reproduction of Daphnia galeata. J. Chem. Ecol. 30:483–500.PubMedCrossRefGoogle Scholar
  42. Martin-Creuzburg, D., Wacker, A., and Von Elert, E. 2005a. Life history consequences of sterol availability in the aquatic keystone species Daphnia. Oecologia 144:362–372.CrossRefGoogle Scholar
  43. Martin-Creuzburg, D., Bec, A., and Von Elert, E. 2005b. Trophic upgrading of picocyanobacterial carbon by ciliates for nutrition of Daphnia magna. Aquat. Microb. Ecol. 41:271–280.CrossRefGoogle Scholar
  44. Martin-Creuzburg, D., Bec, A., and Von Elert, E. 2006. Supplementation with sterols improves food quality of a ciliate for Daphnia magna. Protist 157:477–486.PubMedCrossRefGoogle Scholar
  45. Martin-Creuzburg, D., Westerlund, S.A., and Hoffmann, K.H. 2007. Ecdysteroid levels in Daphnia magna during a molt cycle: determination by radioimmunoassay (RIA) and liquid chromatography-mass spectrometry (LC-MS). Gen. Comp. Endocrinol. 151:66–71.PubMedCrossRefGoogle Scholar
  46. Merris, M., Kraeft, J., Tint, G.S., and Lenard, J. 2004. Long-term effects of sterol depletion in C. elegans: sterol content of synchronized wild-type and mutant populations. J. Lipid Res. 45:2044–2051.PubMedCrossRefGoogle Scholar
  47. Moreau, R.A., Whitaker, B.D., and Hicks, K.B. 2002. Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and health-promoting uses. Prog. Lipid Res. 41:457–500.PubMedCrossRefGoogle Scholar
  48. Müller-Navarra, D.C., Brett, M., Liston, A.M., and Goldman, C.R. 2000. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77.PubMedCrossRefGoogle Scholar
  49. Nes, W.R., and McKean, M.L. 1977. Biochemistry of steroids and other isopentenoids. University Park Press, Baltimore, MD.Google Scholar
  50. Normén, L., Shaw, C.A., Fink, C.S., and Awad, A.B. 2004. Combination of phytosterols and omega-3 fatty acids: A potential strategy to promote cardiovascular health. Curr. Med. Chem. Cardiovasc. Hematol. Agents 2:1–12.PubMedCrossRefGoogle Scholar
  51. Ohvo-Rekilä, H., Ramstedt, B., Leppimäki, P., and Slotte, P. 2002. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41:66–97.PubMedCrossRefGoogle Scholar
  52. Oliver, R.L., and Ganf, G.G. 2000. Freshwater blooms, pp. 149–194. In B.A. Whitton (ed.), The ecology of cyanobacteria: their diversity in time and space. Kluwer, Dordrecht.Google Scholar
  53. Ourisson, G., Rohmer, M., and Poralla, K. 1987. Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Ann. Rev. Microbiol. 41:301–333.CrossRefGoogle Scholar
  54. Patterson, G.W. 1991. Sterols of algae, pp. 118–157. In G.W. Patterson, and W.D. Nes (eds.), Physiology and biochemistry of sterols. American Oil Chemists’ Society, Champaign, IL.Google Scholar
  55. Patterson, G.W., Tsitsa-Tzardis, E., Wikfors, G.H., Ghosh, P., Smith, B. C., and Gladu, P.K. 1994. Sterols of eustigmatophytes. Lipids 29:661–664.PubMedCrossRefGoogle Scholar
  56. Piironen, V., Lindsay, D., Miettinen, T., Toivo, J., and Lampi, A.M. 2000. Plant sterols: biosynthesis, biological function and their importance to human nutrition. J. Sci. Food Agric. 80:939–966.CrossRefGoogle Scholar
  57. Popov, S., Stoilov, I., Marekov, N., Kovachev, G., and Andreev, S. 1981. Sterols and their biosynthesis in some freshwater bivalves. Lipids 16:663–669.CrossRefGoogle Scholar
  58. Porter, J.A., Young, K.E., and Beachy, P.A. 1996. Cholesterol modification of hedgehog signaling proteins in animal development. Science 274:255–259.PubMedCrossRefGoogle Scholar
  59. Prahl, F.G., Eglinton, G., Corner, E.D.S., O’Hara, S.C.M., and Forsberg, T.E.V. 1984. Changes in plant lipids during passage through the gut of Calanus. J. Mar. Biol. Ass. U. K. 64:317–334.CrossRefGoogle Scholar
  60. Raederstorff, D., and Rohmer, M. 1987. Sterol biosynthesis via cycloartenol and other biochemical features related to photosynthetic phyla in the amoebae Naegleria lovaniensis and Naegleria gruberi. Eur. J. Biochem. 164:427–434.PubMedCrossRefGoogle Scholar
  61. Raederstorff, D., and Rohmer, M. 1988. Polyterpenoids as cholesterol and tetrahymanol surrogates in the ciliate Tetrahymena pyriformis. Biochim. Biophys. Acta 960:190–199.PubMedGoogle Scholar
  62. Rohmer, M., Knani, M., Simonin, P., Sutter, B., and Sahm, H. 1993. Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J. 295:517–524.PubMedGoogle Scholar
  63. Schaller, H. 2003. The role of sterols in plant growth and development. Prog. Lipid Res. 42:163–175.PubMedCrossRefGoogle Scholar
  64. Shim, Y.-H., Chun, J.H., Lee, E.-Y., and Paik, Y.-K. 2002. Role of cholesterol in germ-line development of Caenorhabditis elegans. Mol. Reprod. Dev. 61:358–366.PubMedCrossRefGoogle Scholar
  65. Silva, C.J., Wünsche, L., and Djierassi, C. 1991. Biosynthetic studies of marine lipids 35. The demonstration of de novo sterol biosynthesis in sponges using radiolabeled isoprenoid precursors. Comp. Biochem. Physiol. 99B:763–773.Google Scholar
  66. Soudant, P., Le Coz, J.-R., Marty, Y., Moal, J., Robert, R., and Samain, J.-F. 1998. Incorporation of microalgae sterols by scallop Pecten maximus (L.) larvae. Comp. Biochem. Physiol. A. 119:451–457.Google Scholar
  67. Stoecker, D.K., and Capuzzo, J.M. 1990. Predation on Protozoa: its importance to zooplankton. J. Plankton Res. 12:891–908.CrossRefGoogle Scholar
  68. Summons, R.E., Bradley, A.S., Jahnke, L.L., and Waldbauer, J.R. 2006. Steroids, triterpenoids and molecular oxygen. Phil. Trans. R. Soc. B 361:951–968.PubMedCrossRefGoogle Scholar
  69. Svoboda, J.A., and Thompson, M.J. 1985. Steroids, pp. 137–175. In G.A. Kerkut, and L.I. Gilbert (eds.). Comprehensive insect physiology, biochemistry and pharmacology. Pergamon, New York.Google Scholar
  70. Teshima, S.-I. 1971. Bioconversion of β-sitosterol and 24-methylcholesterol to cholesterol in marine crustacea. Comp. Biochem. Physiol. 39B:815–822.Google Scholar
  71. Teshima, S.-I. 1991. Sterols of crustaceans, molluscs and fish, pp. 229–256. In G.W. Patterson, and W.D. Nes (eds.), Physiology and biochemistry of sterols. American Oil Chemists’ Society, Champaign, IL.Google Scholar
  72. Thompson Jr., G.A. 1996. Lipids and membrane function in green algae. Biochim. Biophys. Acta 1302:17–45.PubMedGoogle Scholar
  73. Trautwein, E.A., Duchateau, G.S.M.J.E., Lin, Y., Mel’nikov, S., Molhuizen, H.O.F., and Ntanios, F.Y. 2003. Proposed mechanisms of cholesterol-lowering action of plant sterols. Eur. J. Lipid Sci. Technol. 105:171–185.CrossRefGoogle Scholar
  74. Trider, D.J., and Castell, J.D. 1980. Effect of dietary lipids on growth tissue composition and metabolism of the oyster (Crassostrea virginica). J. Nutr. 110:1303–1309.PubMedGoogle Scholar
  75. Tsitsa-Tzardis, S.E., Patterson, G.W., Wikfors, G.H., Gladu, P.K., and Harrison, D. 1993. Sterols of Chaetoceros and Skeletonema. Lipids 28:465–467.CrossRefGoogle Scholar
  76. VanWagtendonk, W.J. 1974. Nutrition of Paramecium, pp. 339–376. In W.J. VanWagtendonk (ed.), Paramecium, a current survey. Elsevier, Amsterdam.Google Scholar
  77. Véron, B., Dauguet, J.-C., and Billard, C. 1998. Sterolic biomarkers in marine phytoplankton. II. Free and conjugated sterols of seven species used in mariculture. J. Phycol. 34:273–279.CrossRefGoogle Scholar
  78. Volkman, J.K. 2003. Sterols in microorganisms. Appl. Microbiol. Biotech. 60:495–506.Google Scholar
  79. Volkman, J.K. 2005. Sterols and other triterpenoids: source specificity and evolution of biosynthetic pathways. Org. Geochem. 36:139–159.CrossRefGoogle Scholar
  80. Volkman, J.K., Barrett, S.M., Blackburn, S.I., Mansour, M.P., Sikes, E.L., and Gelin, F. 1998. Microalgal biomarkers: a review of recent research developments. Org. Geochem. 29:1163–1179.CrossRefGoogle Scholar
  81. Von Elert, E. 2002. Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol. Oceanogr. 47:1764–1773.CrossRefGoogle Scholar
  82. Von Elert, E., Martin-Creuzburg, D., and Le Coz, J.R. 2003. Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc. R. Soc. Lond. B Bio. 270:1209–1214.CrossRefGoogle Scholar
  83. Voogt, P.A. 1975. Investigations of the capacity of synthesizing 3β-sterols in Mollusca-XIII. Biosynthesis and composition of sterols in some bivalves (Anisomyaria). Comp. Biochem. Physiol. 50B:499–504.Google Scholar
  84. Wacker, A., and Martin-Creuzburg, D. 2007. Allocation of essential lipids in Daphnia magna during exposure to poor food quality. Funct. Ecol. 21:738–747.CrossRefGoogle Scholar
  85. Williams, B.L., Goodwin, T.W., and Ryley, J.F. 1966. The sterols of some protozoa. J. Protozool. 13:227–230.PubMedGoogle Scholar
  86. Wright, D.C., Berg, L.R., and Patterson, G.W. 1980. Effect of culture conditions on the sterols and fatty acids of green algae. Phytochemistry 19:783–785.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Limnological InstituteUniversity of ConstanceKonstanzGermany

Personalised recommendations