A key process in freshwater plankton food webs is the regulation of the efficiency of energy and material transfer. Cyanobacterial carbon (C) in particular is transferred very inefficiently to herbivorous zooplankton, which leads to a decoupling of primary and secondary production and the accumulation of cyanobacterial biomass, which is associated with reduced recreational quality of water bodies and hazards to human health. A recent correlative field study suggested that the low transfer efficiency of cyanobacterial C is the result of the absence of long–chain polyunsaturated fatty acids (PUFA) in the diet of the zooplankton. By supplementation of single–lipid compounds in controlled growth experiments, we show here that the low C transfer efficiency of coccal and filamentous cyanobacteria to the keystone herbivore Daphnia is caused by the low sterol content in cyanobacteria, which constrains cholesterol synthesis and thereby growth and reproduction of the herbivore. Estimations of sterol requirement in Daphnia suggest that, when cyanobacteria comprise more than 80% of the grazed phytoplankton, growth of the herbivore may be limited by sterols and Daphnia may subsequently fail to control phytoplankton biomass. Dietary sterols therefore may play a key role in freshwater food webs and in the control of water quality in lakes dominated by cyanobacteria.

Summary: In nature, food conditions change temporally and force consumers into trade‐offs during resource allocation. In particular, under poor food conditions, for example during cyanobacterial blooms, herbivores have to optimize their resource allocation to maximize fitness, and face two decisions: (i) an individual might attempt to allocate acquired essential resources to reproductive tissues or use them for its own maintenance; and (ii) an individual might decide to optimize the chemical quality of its eggs. As cyanobacteria feature a deficiency in some essential lipids that leads to a decline in the growth and fecundity of Daphnia, an important freshwater herbivore, we investigated Daphnia magna's Strauss allocation of lipids such as polyunsaturated fatty acids (PUFAs) and cholesterol during an experimental non‐toxic cyanobacterial bloom. Generally, we found a substantial maternal investment of the particularly important omega‐3 (n‐3) PUFAs, in particular eicosapentaenoic acid (EPA), into the eggs. The concentration of EPA was 2·4‐fold higher in eggs than in somatic tissue, a cumulative effect, which was not significantly changed under cyanobacterial food conditions. Under poor conditions, D. magna not only decreased the number of eggs produced but, in principle, reduced the previously high concentrations of EPA in both eggs and somatic tissues to a similar degree. In contrast to EPA, the concentrations of α‐linolenic acid and cholesterol, although lower than EPA, were more homeostatic in eggs than in somatic tissues, in which concentrations decreased. When food quality was improved, D. magna were able to recover completely the fatty acid concentrations in their somatic tissues and eggs. This study shows that the content of particular lipids in its food clearly affects resource allocation in D. magna, and suggests that cholesterol is important for somatic growth, while PUFAs are primarily needed for reproduction. As a decreasing investment of essential lipids into eggs implies a reduced fitness of the animals’ progeny under poor food conditions, this could have a strong impact on population dynamics, which might also be valid for other species.

Empirical data providing evidence for a colimitation of an herbivore by two or more essential nutrients are scarce, particularly in regard to biochemical resources. Here, a graphical model is presented, which describes the growth of an herbivore in a system with two potentially limiting resources. To verify this model, life-history experiments were conducted with the herbivore Daphnia magna feeding on the picocyanobacterium Synechococcus elongatus , which was supplemented with increasing amounts of cholesterol either in the presence or the absence of saturating amounts of eicosapentaenoic acid (EPA). For comparison, D. magna was raised on diets containing different proportions of S. elongatus and the cholesterol- and EPA-rich eukaryotic alga Nannochloropsis limnetica . Somatic and population growth of D. magna on a sterol- and EPA-deficient diet was initially constrained by the absence of sterols. With increased sterol availability, a colimitation by EPA became apparent and when the sterol requirements were met, the growth-limiting factor was shifted from a limitation by sterols to a limitation by EPA. These data imply that herbivores are frequently limited by two or more essential nutrients simultaneously. Hence, the concept of colimitation has to be incorporated into models assessing nutrient-limited growth kinetics of herbivores to accurately predict demographic changes and population dynamics.

We investigated whether trophic repackaging of autotrophic picoplankton by phagotrophic protists is associated with an improvement in food quality for the metazooplankton Daphnia magna (i.e., whether trophic upgrading occurs in this system). The nutritional value of the autotrophic species Microcystis aeruginosa PCC7806, Synechococcus sp. strain BO8809, Synechococcus elongatus SAG 89.79, and Choricystis minor KR1988/ 8, and of the heterotrophic nanoflagellate Paraphysomonas sp. grown on these different picoplanktonic species was evaluated in standardized growth experiments with D. magna. In order to investigate the functional role of the flagellate in the simplified autotrophic picoplankton‐Daphnia food chain, Paraphysomonas sp. was grown on the different picoplanktonic organisms and subsequently separated from the food items before being fed to D. magna. The presence of Paraphysomonas sp. as an intermediary trophic step enhanced somatic growth and reproduction of D. magna. Supplementation of Synechococcus sp. with lipids from Paraphysomonas sp. (grown on Synechococcus sp.) revealed that trophic upgrading of autotrophic picoplankton is due to the additional lipids present in the flagellate. Paraphysomonas sp. synthesized polyunsaturated fatty acids and sterols de novo, which most likely explains the trophic upgrading. Paraphysomonas sp. also improved the food quality of M. aeruginosa PCC7806, which is toxic for D. magna. The heterotrophic flagellate Paraphysomonas sp. is capable of trophically upgrading a poor quality food source not only by producing essential lipids, but also by detoxifying the cyanobacterial food organism.