Nutritional constraints at the cyanobacteria–Daphnia magna interface: The role of sterols

In past decades, a considerable amount of research has been conducted to elucidate the factors that affect the carbon transfer across the cyanobacteria–Daphnia interface. It is well accepted that cyanobacteria are a nutritionally inadequate food source for cladocerans, but the underlying mechanisms are still controversial. Morphological properties, toxicity, and the absence of essential lipids, i.e., polyunsaturated fatty acids (PUFAs) and sterols, are discussed as the most important factors that account for this nutritional inadequacy. Here, we conducted standardized growth experiments with the herbivore Daphnia magna feeding on coccal, filamentous, and putatively toxic cyanobacterial strains comprising the genera Synechococcus, Anabaena, Aphanizomenon, and Microcystis and on a cyanobacterial mixture containing strains of these genera. The relative importance of PUFAs and sterols in determining the food quality of cyanobacteria for Daphnia was assessed by supplementation of eicosapentaenoic acidand/or cholesterol-containing liposomes to the cyanobacterial carbon. We provide evidence that somatic growth of daphnids on coccal as well as on filamentous cyanobacteria is primarily constrained by the absence of sterols, provided that the cyanobacterial carbon is readily ingested and nontoxic. The absence of PUFAs in cyanobacteria appears to be of minor importance for somatic growth but potentially affects egg production in Daphnia. Thus, the absence of sterols has to be considered a major food-quality constraint that potentially affects the efficiency of carbon transfer across the cyanobacteria–Daphnia interface. Trophic interactions at the autotroph–herbivore interface significantly affect the efficiency of carbon transfer to higher trophic levels in freshwater ecosystems. Cladocerans of the genus Daphnia are the dominant herbivores in lakes and ponds; owing to their abundance and their high grazing activity on the phytoplankton they provide a crucial link between primary and secondary production. However, the carbon transfer efficiency at the phytoplankton– Daphnia interface is often constrained by the predominance of nutritionally inadequate food sources. Cyanobacteria are well known for their nutritional inadequacy for freshwater cladocerans (De Bernardi and Giussani 1990; Wilson et al. 2006). In particular in eutrophic lakes, where cyanobacteria often dominate the phytoplankton, carbon is transferred inefficiently to crustacean grazers. As a result, an accumulation of cyanobacterial biomass occurs (cyanobacterial bloom), which is often associated with hazards to human health and livestock and reduced recreational quality of water bodies (Carmichael 1994). In past decades, reasons determining the low assimilation of cyanobacterial carbon by Daphnia have been extensively studied, and three major food-quality constraints have been revealed: (1) grazing resistance, (2) toxicity, and (3) a deficiency in essential nutrients. Grazing resistance due to morphological properties, such as the formation of large filaments or cell colonies, is regarded as the most important food-quality constraint. Mechanical interference with the filtering process of daphnids not only hampers ingestion, but also is associated with higher rejection and respiration rates and, therewith, increased energetic costs (Porter and McDonough 1984). Large Daphnia species (e.g., Daphnia magna) have been shown to be more sensitive to filamentous cyanobacteria than smaller sized Daphnia species because of their larger carapace gap, i.e., smaller sized Daphnia have a greater ability to avoid the filtration of large filaments. This might also explain the often observed shift from largeto small-bodied cladocerans during cyanobacterial bloom conditions (Porter and McDonough 1984; DeMott et al. 2001). Toxin production has been reported in a large number of cyanobacterial species. Toxin content, however, varies significantly among strains and even between clones of the same isolate (Dow and Swoboda 2000). Conventional1 To whom correspondence should be addressed. Present address: Limnological Institute, Mainaustrasse 252, University of Constance, 78464 Konstanz, Germany (Dominik.Martin-Creuzburg@ uni-konstanz.de) Acknowledgments We thank P. Merkel and C. Gebauer for excellent technical assistance and two anonymous reviewers for valuable comments on an earlier draft of this manuscript. This study was supported by the German Research Foundation (DFG, Graduate College 678/2). Limnol. Oceanogr., 53(2), 2008, 456–468 E 2008, by the American Society of Limnology and Oceanography, Inc.