Skip to main content
Log in

Thresholds for Sterol-Limited Growth of Daphnia magna: A Comparative Approach Using 10 Different Sterols

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Arthropods are incapable of synthesizing sterols de novo and thus require a dietary source to cover their physiological demands. The most prominent sterol in animal tissues is cholesterol, which is an indispensable structural component of cell membranes and serves as precursor for steroid hormones. Instead of cholesterol, plants and algae contain a variety of different phytosterols. Consequently, herbivorous arthropods have to metabolize dietary phytosterols to cholesterol to meet their requirements for growth and reproduction. Here, we investigated sterol-limited growth responses of the freshwater herbivore Daphnia magna by supplementing a sterol-free diet with increasing amounts of 10 different phytosterols and comparing thresholds for sterol-limited growth. In addition, we analyzed the sterol composition of D. magna to explore sterol metabolic constraints and bioconversion capacities. We show that dietary phytosterols strongly differ in their potential to support somatic growth of D. magna. The dietary threshold concentrations obtained by supplementing the different sterols cover a wide range (3.5–34.4 μg mg C−1) and encompass the one for cholesterol (8.9 μg mg C−1), indicating that certain phytosterols are more efficient in supporting somatic growth than cholesterol (e.g., fucosterol, brassicasterol) while others are less efficient (e.g., dihydrocholesterol, lathosterol). The dietary sterol concentration gradients revealed that the poor quality of particular sterols can be alleviated partially by increasing dietary concentrations, and that qualitative differences among sterols are most pronounced at low to moderate dietary concentrations. We infer that the dietary sterol composition has to be considered in zooplankton nutritional ecology to accurately assess potential sterol limitations under field conditions.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson TR, Hessen DO, Elser JJ, Urabe J (2005) Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am Nat 165:1–15

    Article  PubMed  Google Scholar 

  • Basen T, Rothhaupt K-O, Martin-Creuzburg D (2012) Absence of sterols constrains food quality of cyanobacteria for an invasive freshwater bivalve. Oecologia 170:57–64

    Article  PubMed  Google Scholar 

  • Bec A, Martin-Creuzburg D, von Elert E (2006) Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnol Oceanogr 51:1699–1707

    Article  Google Scholar 

  • Behmer ST, Elias DO, Bernays EA (1999a) Post-ingestive feedbacks and associative learning regulate the intake of unsuitable sterols in a generalist grasshopper. J Exp Biol 202:739–748

    PubMed  CAS  Google Scholar 

  • Behmer ST, Elias DO, Grebenok RJ (1999b) Phytosterol metabolism and absorption in the generalist grasshopper, Schistocerca americana (Orthoptera : Acrididae). Arch Insect Biochem Physiol 42:13–25

    Article  PubMed  CAS  Google Scholar 

  • Behmer ST, Grebenok RJ, Douglas AE (2011) Plant sterols and host plant suitability for a phloem-feeding insect. Funct Ecol 25:484–491

    Article  Google Scholar 

  • Behmer ST, Nes WD (2003) Insect sterol nutrition and physiology: A global overview. Adv Insect Physiol 31:1–72

    Article  CAS  Google Scholar 

  • Bertalanffy LV (1957) Quantitative laws in metabolism and growth. Q Rev Biol 32:217–231

    Article  Google Scholar 

  • Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton

    Google Scholar 

  • Carvalho M et al (2010) Survival strategies of a sterol auxotroph. Development 137:3675–3685

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chamberlain PM, Bull ID, Black HIJ, Ineson P, Evershed RP (2004) Lipid content and carbon assimilation in Collembola: implications for the use of compound-specific carbon isotope analysis in animal dietary studies. Oecologia 139:325–335

    Article  PubMed  Google Scholar 

  • Clayton RB (1960) The role of intestinal symbionts in the sterol metabolism of Blattella germanica. J Biol Chem 235:3421–3425

    PubMed  CAS  Google Scholar 

  • Entchev EV, Kurzchalia TV (2005) Requirement of sterols in the life cycle of the nematode Caenorhabditis elegans. Semin Cell Dev Biol 16:175–182

    Article  PubMed  CAS  Google Scholar 

  • Giner JL, Faraldos JA, Boyer GL (2003) Novel sterols of the toxic dinoflagellate Karenia brevis (Dinophyceae): A defensive function for unusual marine sterols? J Phycol 39:315–319

    Article  CAS  Google Scholar 

  • Goad LJ (1981) Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl Chem 53:837–852

    Article  CAS  Google Scholar 

  • Grieneisen ML (1994) Recent advances in our knowledge of ecdysteroid biosynthesis in insects and crustaceans. Insect Biochem Molec Biol 24:115–132

    Article  CAS  Google Scholar 

  • Haines TH (2001) Do sterols reduce proton and sodium leaks through lipid bilayers? Prog Lipid Res 40:299–324

    Article  PubMed  CAS  Google Scholar 

  • Harvey HR, Eglinton G, O’Hara SCM, Corner EDS (1987) Biotransformation and assimilation of dietary lipids by Calanus feeding on a dinoflagellate. Geochim Cosmochim Acta 51:3031–3040

    Article  Google Scholar 

  • Hassett RP (2004) Supplementation of a diatom diet with cholesterol can enhance copepod egg-production rates. Limnol Oceanogr 49:488–494

    Article  CAS  Google Scholar 

  • Ikekawa N, Morisaki M, Fujimoto Y (1993) Sterol metabolism in insects: Dealkylation of phytosterol to cholesterol. Accounts Chem Res 26:139–146

    Article  CAS  Google Scholar 

  • Kanazawa A (2001) Sterols in marine invertebrates. Fisheries Sci 67:997–1007

    Article  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 

  • Lampert W (1991) The dynamics of Daphnia in a shallow lake. Verh Int Ver Limnol 24:795–798

    Google Scholar 

  • Lukas M, Wacker A (2014) Daphnia’s dilemma: adjustment of carbon budgets in the face of food and cholesterol limitation. J Exp Biol 217:1079–1086

    Article  PubMed  Google Scholar 

  • Martin-Creuzburg D, Bec A, von Elert E (2005a) Trophic upgrading of picocyanobacterial carbon by ciliates for nutrition of Daphnia magna. Aquat Microb Ecol 41:271–280

    Article  Google Scholar 

  • Martin-Creuzburg D, Beck B, Freese HM (2011) Food quality of heterotrophic bacteria for Daphnia magna: evidence for a limitation by sterols. FEMS Microbiol Ecol 76:592–601

    Article  PubMed  Google Scholar 

  • Martin-Creuzburg D, Sperfeld E, Wacker A (2009) Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proc R Soc B 276:1805–1814

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Martin-Creuzburg D, von Elert E (2004) Impact of 10 dietary sterols on growth and reproduction of Daphnia galeata. J Chem Ecol 30:483–500

    Article  PubMed  CAS  Google Scholar 

  • Martin-Creuzburg D, von Elert E (2009) Ecological significance of sterols in aquatic food webs. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 43–64

    Chapter  Google Scholar 

  • Martin-Creuzburg D, von Elert E, Hoffmann KH (2008) Nutritional constraints at the cyanobacteria-Daphnia magna interface: The role of sterols. Limnol Oceanogr 53:456–468

    Article  Google Scholar 

  • Martin-Creuzburg D, Wacker A, Basen T (2010) Interactions between limiting nutrients: Consequences for somatic and population growth of Daphnia magna. Limnol Oceanogr 55:2597–2607

    Article  CAS  Google Scholar 

  • Martin-Creuzburg D, Wacker A, von Elert E (2005b) Life history consequences of sterol availability in the aquatic keystone species Daphnia. Oecologia 144:362–372

    Article  PubMed  Google Scholar 

  • Martin-Creuzburg D, Wacker A, Ziese C, Kainz MJ (2012) Dietary lipid quality affects temperature-mediated reaction norms of a freshwater key herbivore. Oecologia 168:901–912

    Article  PubMed  Google Scholar 

  • Moreau RA, Whitaker BD, Hicks KB (2002) Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and health-promoting uses. Prog Lipid Res 41:457–500

    Article  PubMed  CAS  Google Scholar 

  • Nasir H, Noda H (2003) Yeast-like symbiotes as a sterol source in anobiid beetles (Coleoptera, Anobiidae): Possible metabolic pathways from fungal sterols to 7-dehydrocholesterol. Arch Insect Biochem Physiol 52:175–182

    Article  PubMed  CAS  Google Scholar 

  • Ohvo-Rekilä H, Ramstedt B, Leppimäki P, Slotte JP (2002) Cholesterol interactions with phospholipids in membranes. Prog Lipid Res 41:66–97

    Article  PubMed  Google Scholar 

  • Piepho HP (2004) An algorithm for a letter-based representation of all-pairwise comparisons. J Comput Graph Stat 13:456–466

    Article  Google Scholar 

  • Piepho M, Martin-Creuzburg D, Wacker A (2010) Simultaneous effects of light intensity and phosphorus supply on the sterol content of phytoplankton. PLoS ONE 5:e15828

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Porter JA, Young KE, Beachy PA (1996) Cholesterol modification of hedgehog signaling proteins in animal development. Science 274:255–259

    Article  PubMed  CAS  Google Scholar 

  • Prahl FG, Eglinton G, Corner EDS, O’Hara SCM, Forsberg TEV (1984) Changes in plant lipids during passage through the gut of Calanus. J Mar Biol Assoc UK 64:317–334

    Article  CAS  Google Scholar 

  • Sakurai S, Yonemura N, Fujimoto Y, Hata F, Ikekawa N (1986) 7-dehydrosterols in prothoracic glands of the silkworm, Bombyx mori. Experientia 42:1034–1036

    Article  CAS  Google Scholar 

  • Sperfeld E, Martin-Creuzburg D, Wacker A (2012) Multiple resource limitation theory applied to herbivorous consumers: Liebig’s minimum rule vs. interactive co-limitation. Ecol Lett 15:142–150

    Article  PubMed  Google Scholar 

  • Sperfeld E, Wacker A (2009) Effects of temperature and dietary sterol availability on growth and cholesterol allocation of the aquatic keystone species Daphnia. J Exp Biol 212:3051–3059

    Article  PubMed  CAS  Google Scholar 

  • Sperfeld E, Wacker A (2011) Temperature- and cholesterol-induced changes in eicosapentaenoic acid limitation of Daphnia magna determined by a promising method to estimate growth saturation thresholds. Limnol Oceanogr 56:1273–1284

    Article  CAS  Google Scholar 

  • Svoboda JA (1999) Variability of metabolism and function of sterols in insects. Crit Rev Biochem Mol 34:49–57

    Article  CAS  Google Scholar 

  • Thompson GA (1996) Lipids and membrane function in green algae. Biochim Biophys Acta 1302:17–45

    Article  PubMed  Google Scholar 

  • Volkman JK (2003) Sterols in microorganisms. Appl Microbiol Biot 60:495–506

    Article  CAS  Google Scholar 

  • Wacker A, Martin-Creuzburg D (2012) Biochemical nutrient requirements of the rotifer Brachionus calyciflorus: co-limitation by sterols and amino acids. Funct Ecol 26:1135–1143

    Article  Google Scholar 

Download references

Acknowledgments

We thank P. Merkel for technical assistance in analyzing sterols. DMC was supported financially by the ‘Young Scholar Fund’ of the University of Konstanz, AW was supported by the German Research Foundation (DFG, WA 2,445/8-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dominik Martin-Creuzburg.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 107 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin-Creuzburg, D., Oexle, S. & Wacker, A. Thresholds for Sterol-Limited Growth of Daphnia magna: A Comparative Approach Using 10 Different Sterols. J Chem Ecol 40, 1039–1050 (2014). https://doi.org/10.1007/s10886-014-0486-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-014-0486-1

Keywords

Navigation