Skip to main content
Log in

Maternal diet of Daphnia magna affects offspring growth responses to supplementation with particular polyunsaturated fatty acids

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Previous studies examining the effects of food quality on zooplankton often controlled for maternal effects of resource provisioning using standardized maternal diets. However, varying nutritional history of mothers may change resource provisioning to their progeny, especially regarding polyunsaturated fatty acids (PUFAs), which may change the interpretation of previously observed fitness responses of offspring. To assess PUFA-mediated maternal provisioning effects on offspring, we raised females of the cladoceran Daphnia magna on diets differing considerably in PUFA composition and raised their offspring on a PUFA-lacking diet supplemented with the ω3 PUFAs α-linolenic acid (ALA) and/or eicosapentaenoic acid (EPA). The mass-specific growth responses of offspring to their own diets were affected by the maternal diet regime, probably due to varying maternal PUFA provisioning. A low maternal provisioning of EPA or ALA was sufficient to prevent growth limitation of offspring by these PUFAs until reaching maturity. A comparison with results of published ALA and EPA supplementation experiments suggests that the previously observed limitation effects depended on the usage of a single algae genus as maternal diet. Therefore, we suggest that maternal diets should be deliberately varied in future studies assessing ecological relevant food quality effects on zooplankton, especially regarding PUFAs.

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

  • Agrawal, A. A., C. Laforsch & R. Tollrian, 1999. Transgenerational induction of defences in animals and plants. Nature 401: 60–63.

    Article  CAS  Google Scholar 

  • Alekseev, V. & W. Lampert, 2001. Maternal control of resting-egg production in Daphnia. Nature 414: 899–901.

    Article  CAS  PubMed  Google Scholar 

  • Becker, C. & M. Boersma, 2003. Resource quality effects on life histories of Daphnia. Limnology & Oceanography 48: 700–706.

    Article  Google Scholar 

  • Becker, C. & M. Boersma, 2005. Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnology & Oceanography 50: 388–397.

    Article  CAS  Google Scholar 

  • Becker, C. & M. Boersma, 2007. Effects of essential fatty acids on the reproduction of a generalist herbivore. Journal of Plankton Research 29: 463–470.

    Article  CAS  Google Scholar 

  • Boersma, M., 1997. Offspring size and parental fitness in Daphnia magna. Evolutionary Ecology 11: 439–450.

    Article  Google Scholar 

  • Boersma, M., 2000. The nutritional quality of P-limited algae for Daphnia. Limnology & Oceanography 45: 1157–1161.

    Article  CAS  Google Scholar 

  • Boersma, M. & C. Kreutzer, 2002. Life at the edge: Is food quality really of minor importance at low quantities? Ecology 83: 2552–2561.

    Article  Google Scholar 

  • Brett, M. T., 1993. Resource quality effects on Daphnia longispina offspring fitness. Journal of Plankton Research 15: 403–412.

    Article  Google Scholar 

  • Brzezinski, T. & E. Von Elert, 2007. Biochemical food quality effects on a Daphnia hybrid complex. Limnology & Oceanography 52: 2350–2357.

    Article  Google Scholar 

  • Frost, P. C., D. Ebert, J. H. Larson, M. A. Marcus, N. D. Wagner & A. Zalewski, 2010. Transgenerational effects of poor elemental food quality on Daphnia magna. Oecologia 162: 865–872.

    Article  PubMed  Google Scholar 

  • Glazier, D. S., 1992. Effects of food, genotype, and maternal size and age on offspring investment in Daphnia magna. Ecology 73: 910–926.

    Article  Google Scholar 

  • Guillard, R. R., 1975. Cultures of phytoplankton for feeding of marine invertebrates. In Smith, W. L. & M. H. Chanley (eds), Culture of marine invertebrate animals. Plenum Press, New York: 26–60.

    Google Scholar 

  • Guisande, C. & Z. M. Gliwicz, 1992. Egg size and clutch size in two Daphnia species grown at different food levels. Journal of Plankton Research 14: 997–1007.

    Article  Google Scholar 

  • Hartwich, M., D. Martin-Creuzburg, K.-O. Rothhaupt & A. Wacker, 2012. Oligotrophication of a large, deep lake alters food quantity and quality constraints at the primary producer–consumer interface. Oikos 121: 1702–1712.

    Article  CAS  Google Scholar 

  • Hartwich, M., D. Martin-Creuzburg & A. Wacker, 2013. Seasonal changes in the accumulation of polyunsaturated fatty acids in zooplankton. Journal of Plankton Research 35: 121–134.

    Article  CAS  Google Scholar 

  • Hassett, R. P. & E. L. Crockett, 2009. Habitat temperature is an important determinant of cholesterol contents in copepods. The Journal of Experimental Biology 212: 71–77.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayashi, Y., L. H. Heckmann, A. Callaghan & R. M. Sibly, 2008. Reproduction recovery of the crustacean Daphnia magna after chronic exposure to ibuprofen. Ecotoxicology 17: 246–251.

    Article  CAS  PubMed  Google Scholar 

  • Heckmann, L. H., R. M. Sibly, M. J. T. N. Timmermans & A. Callaghan, 2008. Outlining eicosanoid biosynthesis in the crustacean Daphnia. Frontiers in Zoology 5: 11.

    Article  PubMed Central  PubMed  Google Scholar 

  • Jöhnk, K. D., J. Huisman, J. Sharples, B. Sommeijer, P. M. Visser & J. M. Stroom, 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14: 495–512.

    Article  Google Scholar 

  • Keating, K. I., 1985. The influence of vitamin B12 deficiency on the reproduction of Daphnia pulex Leydig (Cladocera). Journal of Crustacean Biology 5: 130–136.

    Article  CAS  Google Scholar 

  • Koch, U., D. Martin-Creuzburg, H.-P. Grossart & D. Straile, 2011. Single dietary amino acids control resting egg production and affect population growth of a key freshwater herbivore. Oecologia 167: 981–989.

    Article  PubMed  Google Scholar 

  • LaMontagne, J. M. & E. McCauley, 2001. Maternal effects in Daphnia: What mothers are telling their offspring and do they listen? Ecology Letters 4: 64–71.

    Article  Google Scholar 

  • Lampert, W., 1991. The dynamics of Daphnia in a shallow lake. Verhandlungen der internationalen Vereinigung für theoretische und angewandte Limnologie 24: 795–798.

    Google Scholar 

  • Lukas, M., E. Sperfeld & A. Wacker, 2011. Growth Rate Hypothesis does not apply across colimiting conditions: cholesterol limitation affects phosphorus homoeostasis of an aquatic herbivore. Functional Ecology 25: 1206–1214.

    Article  Google Scholar 

  • Martin-Creuzburg, D., E. Sperfeld & A. Wacker, 2009. Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proceedings of the Royal Society of London Series B: Biological Sciences 276: 1805–1814.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martin-Creuzburg, D., E. Von Elert & K. H. Hoffmann, 2008. Nutritional constraints at the cyanobacteria-Daphnia magna interface: The role of sterols. Limnology and Oceanography 53: 456–468.

    Article  Google Scholar 

  • Martin-Creuzburg, D., A. Wacker & T. Basen, 2010. Interactions between limiting nutrients and associated consequences for growth and reproduction of Daphnia magna. Limnology & Oceanography 55: 2597–2607.

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • McGinley, M. A., D. H. Temme & M. A. Geber, 1987. Parental investment in offspring in variable environments: theoretical and empirical considerations. The American Naturalist 130: 370–398.

    Article  Google Scholar 

  • Metcalfe, N. B. & P. Monaghan, 2001. Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution 16: 254–260.

    Article  Google Scholar 

  • Mousseau, T. A. & C. W. Fox, 1998. The adaptive significance of maternal effects. Trends in Ecology & Evolution 13: 403–407.

    Article  CAS  Google Scholar 

  • Müller-Navarra, D. C., 1995. Biochemical versus mineral limitation in Daphnia. Limnology & Oceanography 40: 1209–1214.

    Article  Google Scholar 

  • Müller-Navarra, D. C., 2006. The nutritional importance of polyunsaturated fatty acids and their use as trophic markers for herbivorous zooplankton: Does it contradict? Archiv für Hydrobiologie 167: 501–513.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2008. Climate: Blooms like it hot. Science 320: 57–58.

    Article  CAS  PubMed  Google Scholar 

  • Pajk, F., E. Von Elert & P. Fink, 2012. Interaction of changes in food quality and temperature reveals maternal effects on fitness parameters of a keystone aquatic herbivore. Limnology & Oceanography 57: 281–292.

    Google Scholar 

  • Persson, J. & T. Vrede, 2006. Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position. Freshwater Biology 51: 887–900.

    Article  CAS  Google Scholar 

  • R Core Team, 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Ravet, J. L., M. T. Brett & D. C. Müller-Navarra, 2003. A test of the role of polyunsaturated fatty acids in phytoplankton food quality for Daphnia using liposome supplementation. Limnology & Oceanography 48: 1938–1947.

    Article  CAS  Google Scholar 

  • Ravet, J. L., J. Persson & M. T. Brett, 2012. Threshold dietary polyunsaturated fatty acid concentrations for Daphnia pulex growth and reproduction. Inland Waters 2: 199–209.

    Article  CAS  Google Scholar 

  • Rossiter, M., 1996. Incidence and consequences of inherited environmental effects. Annual Review of Ecology and Systematics 27: 451–476.

    Article  Google Scholar 

  • Schlotz, N., J. G. Sørensen & D. Martin-Creuzburg, 2012. The potential of dietary polyunsaturated fatty acids to modulate eicosanoid synthesis and reproduction in Daphnia magna: a gene expression approach. Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 162: 449–454.

    Article  CAS  Google Scholar 

  • Schlotz, N., D. Ebert & D. Martin-Creuzburg, 2013. Dietary supply with polyunsaturated fatty acids and resulting maternal effects influence host-parasite interactions. BMC ecology 13: 41.

    Article  PubMed Central  PubMed  Google Scholar 

  • Schlotz, N., M. Pester, H. M. Freese & D. Martin-Creuzburg, 2014. A dietary polyunsaturated fatty acid improves consumer performance during challenge with an opportunistic bacterial pathogen. FEMS Microbiology Ecology 90: 467–477.

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sperfeld, E. & A. Wacker, 2009. Effects of temperature and dietary sterol availability on growth and cholesterol allocation of the aquatic keystone species Daphnia. The Journal of Experimental Biology 212: 3051–3059.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sperfeld, E. & A. Wacker, 2012. Temperature affects the limitation of Daphnia magna by eicosapentaenoic acid, and the fatty acid composition of body tissue and eggs. Freshwater Biology 57: 497–508.

    Article  CAS  Google Scholar 

  • Stanley-Samuelson, D. W., 1994. The biological significance of prostaglandins and related eicosanoids in invertebrates. American Zoologist 34: 589–598.

    CAS  Google Scholar 

  • Sterner, R. W., 1993. Daphnia growth on varying quality of Scenedesmus: mineral limitation of zooplankton. Ecology 74: 2351–2360.

    Article  Google Scholar 

  • Sundbom, M. & T. Vrede, 1997. Effects of fatty acid and phosphorus content of food on the growth, survival and reproduction of Daphnia. Freshwater Biology 38: 665–674.

    Article  CAS  Google Scholar 

  • Taipale, S. J., M. J. Kainz & M. T. Brett, 2011. Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120: 1674–1682.

    Article  Google Scholar 

  • 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. Limnology & Oceanography 47: 1764–1773.

    Article  Google Scholar 

  • Von Elert, E., 2004. Food quality constraints in Daphnia: interspecific differences in the response to the absence of a long chain polyunsaturated fatty acid in the food source. Hydrobiologia 526: 187–196.

    Article  Google Scholar 

  • Von Elert, E., D. Martin-Creuzburg & J. R. Le Coz, 2003. Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proceedings of the Royal Society of London - Series B: Biological Sciences 270: 1209–1214.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wacker, A. & D. Martin-Creuzburg, 2007. Allocation of essential lipids in Daphnia magna during exposure to poor food quality. Functional Ecology 21: 738–747.

    Article  Google Scholar 

  • Wacker, A. & G. Weithoff, 2009. Carbon assimilation mode in mixotrophs and the fatty acid composition of their rotifer consumers. Freshwater Biology 54: 2189–2199.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Weers, P. M. M., K. Siewertsen & R. D. Gulati, 1997. Is the fatty acids composition of Daphnia galeata determined by the fatty acid composition of the ingested diet? Freshwater Biology 38: 731–738.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Silvia Heim and Sabine Donath for technical assistance. This work was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft, Grant Nos SP1473/1-1 to E.S. and WA2445/8-1 to A.W.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erik Sperfeld.

Additional information

Handling editor: Sigrún Huld Jónasdóttir

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 55 kb)

Supplementary material 2 (DOCX 38 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sperfeld, E., Wacker, A. Maternal diet of Daphnia magna affects offspring growth responses to supplementation with particular polyunsaturated fatty acids. Hydrobiologia 755, 267–282 (2015). https://doi.org/10.1007/s10750-015-2244-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2244-y

Keywords

Navigation