<i>Daphnia</i>'s dilemma of adjusting carbon budgets when facing limitations by food quantity and the essential organic compound cholesterol

Lukas, Marcus; Wacker, Alexander

doi:10.1242/jeb.094151

Cited by 16 publications

(20 citation statements)

References 52 publications

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“…This suggests that a dietary source of sterols is required to maintain basic physiological functions even when the animals are suffering from severe food quantity limitation. Sterols in animals are presumably not burned for gaining energy (Haines, ; Lukas & Wacker, ). Therefore, at low food quantity, the cholesterol provided in our experiment was probably used in physiological processes related to the maintenance of membranes or the production of steroid hormones, whereas fecundity was unaffected.…”

Section: Discussionmentioning

confidence: 99%

“…Most of the existing research on the interplay between food quantity and quality has focused on somatic growth using Daphnia as a model (Boersma & Kreutzer, 2002;Lukas & Wacker, 2014;Sterner & Robinson, 1994). Although rotifers significantly contribute to food web interactions and community dynamics as well, only a few studies have addressed effects of food quantity and quality on population growth of rotifers (Felpeto & Hairston, 2013;Ramos-Rodríguez & Conde-Porcuna, 2003;Štrojsová, Nedoma, Sed'a, & Vrba, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Food quantity–quality co‐limitation: Interactive effects of dietary carbon and essential lipid supply on population growth of a freshwater rotifer

et al. 2019

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Food quantity and quality are highly variable in natural systems. Therefore, their interplay and the associated effects on consumer population growth are important for predator–prey interactions and community dynamics. Experiments in which consumers were exposed to elemental nutrient limitations along food quantity gradients suggest that food quality effects on consumer performance are relevant only at high food quantities. However, elemental nutrients act differently on physiological processes than biochemical nutrients. So far, the interactive effects of food quantity and biochemical compounds on consumer performance have been insufficiently studied. We studied interactive effects of food quantity and biochemical food quality on population growth, including fecundity and survival, of the freshwater rotifer Brachionus calyciflorus. We hypothesised that these life history traits are differently affected by the availability of biochemical nutrients and that food quality effects gain importance with increasing food quantity. In a first experiment, we established food quantity and quality gradients by providing rotifers with different concentrations of a low‐quality food, the sterol‐free cyanobacterium Synechococcus elongatus, supplemented with increasing amounts of cholesterol. In a second experiment, food quantity and quality gradients were established by providing different proportions of two prey species differing in biochemical food quality, i.e. S. elongatus and the lipid‐rich alga Nannochloropsis limnetica, at different total food concentrations. We found that the effects of cholesterol supplementation on population growth increased with increasing food quantity. This interactive effect on population growth was mainly due to food quality effects on fecundity, as effects on survival remained constant along the food quantity gradient. In contrast, when feeding on the mixed algal diet, the food quality effect associated with increasing the proportion of the high‐quality alga did not change along the food quantity gradient. The data on survival and fecundity demonstrate the missing interactive effect of food quantity and quality on population growth, as both traits were oppositely affected. Survival was affected by food quality primarily at low food quantity, whereas food quality effects on fecundity were stronger at high food quantity. Our results highlight the significance of essential biochemicals in mediating the interactive effects of food quantity and quality on population growth. The interplay between food quantity and biochemical food quality limitation seems to influence resource allocation patterns in order to optimise survival or reproduction, which may strongly affect population dynamics in variable environments. As opposed to exploring the function of a single nutrient via supplementation, using algae mixtures allowed us to assess food quality effects on consumer performance in a more natural context by taking potential interactive effects of multiple co‐limiting nutrients into account.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Food quantity–quality co‐limitation: Interactive effects of dietary carbon and essential lipid supply on population growth of a freshwater rotifer

et al. 2019

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“…In contrast to many terrestrial herbivores, daphnids are unselective filter feeders, and thus, presumably unable to equilibrate a dietary mismatch by compensatory feeding or selection of complementary food sources. However, it has been proposed that daphnids are capable of regulating the intake of elemental and essential biochemical nutrients via mechanisms operating post-ingestively in the gut (Anderson et al 2005;Lukas and Wacker 2014).…”

Section: Discussionmentioning

confidence: 99%

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

2014

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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.

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“…In addition to increased ingestion to enhance the assimilation of the limiting food compound, Daphnia may also increase C-releasing processes to get rid of excess dietary C. Feces release is one of those processes and a non-negligible fraction of C is ingested (Lukas and Wacker 2014a). In the present study, we show that the process of feces production is affected differently by different FQ.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies used this model organism to examine the C regulations of herbivorous zooplankton to changing food quality conditions. Increased ingestion rates (P; Darchambeau and Thys 2005) and the high assimilation efficiencies of the limiting food compounds (P; DeMott et al 1998;cholesterol;Lukas and Wacker 2014a) enable Daphnia to adjust to low food quality. Moreover, consumers improve the carbon : nutrient ratio by discharging excess C via feces release, respiration, and excretion of dissolved organic carbon (DOC) (P; Darchambeau et al 2003, Jensen and Hessen 2007, He and Wang 2008cholesterol;Lukas and Wacker 2014a, b).…”

Section: Introductionmentioning

confidence: 99%

Constraints by oxygen and food quality on carbon pathway regulation: a co‐limitation study with an aquatic key herbivore

Lukas

Wacker

2014

Ecology

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In food webs, herbivores are often constrained by low food quality in terms of mineral and biochemical limitations, which in aquatic ecosystems can co‐occur with limited oxygen conditions. As low food quality implies that carbon (C) is available in excess, and therefore a regulation to get rid of excess C is crucial for the performance of consumers, we examined the C pathways (ingestion, feces release, excretion, and respiration) of a planktonic key herbivore (Daphnia magna). We tested whether consumer C pathways increase due to mineral (phosphorus, P) or biochemical (cholesterol and fatty acid) limitations and how these regulations vary when in addition oxygen is low. Under such conditions, at least the capability of the upregulation of respiration may be restricted. Furthermore, we discussed the potential role of the oxygen‐transporting protein hemoglobin (Hb) in the regulation of C budgets. Different food quality constraints led to certain C regulation patterns to increase the removal of excess dietary C: P‐limited D. magna increased excretion and respiration, while cholesterol‐limited Daphnia in addition upregulated the release of feces. In contrast, the regulative effort was low and only feces release increased when D. magna was limited by a long‐chain polyunsaturated fatty acid (eicosapentaenoic acid, EPA). Co‐limiting oxygen did not always impact the discharge of excess C. We found the food‐quality‐induced upregulation of respiration was still present at low oxygen. In contrast, higher excretion of excess C was diminished at low oxygen supply. Besides the effect that the Hb concentration increased under low oxygen, our results indicate a low food‐quality‐induced increase in the Hb content of the animals. Overall, C budgeting is phenotypically plastic towards different (co‐)limiting scenarios. These trigger specific regulation responses that could be the result of evolutionary adaptations.

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Daphnia's dilemma of adjusting carbon budgets when facing limitations by food quantity and the essential organic compound cholesterol

Cited by 16 publications

References 52 publications

Food quantity–quality co‐limitation: Interactive effects of dietary carbon and essential lipid supply on population growth of a freshwater rotifer

Food quantity–quality co‐limitation: Interactive effects of dietary carbon and essential lipid supply on population growth of a freshwater rotifer

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

Constraints by oxygen and food quality on carbon pathway regulation: a co‐limitation study with an aquatic key herbivore

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