Rearing Temperature and Fatty Acid Supplementation Jointly Affect Lipid Fluorescence Polarization and Heat Tolerance in<i>Daphnia</i>

Martin‐Creuzburg, Dominik; Coggins, Bret L.; Ebert, Dieter; Yampolsky, Lev Y.

doi:10.1086/704365

Cited by 20 publications

(27 citation statements)

References 40 publications

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“…That index does consequently not consider fatty acid composition and not account for the concentration of SFAs, which was claimed to be the most common predictor of membrane fluidity (Hazel & Williams, 1990). Still, the calculated UI correlated with membrane fluidity (Martin-Creuzburg et al, 2019). In conclusion, the here observed significant changes in UI and UFA/SFA ratio under simulated DVM (i.e., decreased average temperatures) are in agreement with homeoviscous adaptation of D. magna.…”

Section: Discussionsupporting

confidence: 51%

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The impact of diel vertical migration on fatty acid patterns and allocation inDaphnia magna

Hahn

Elert

2020

PeerJ

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In freshwater zooplankton diel vertical migration (DVM) is a widespread predator-avoidance behavior that is induced by kairomones released from fish. Thereby zooplankton reduces predation by fish by staying in deep and dark colder strata during daytime and migrating into warmer layers during night, and thus experiences diel alterations in temperature. Constantly lower temperatures have been shown to increase the relative abundance of polyunsaturated fatty acids (PUFAs) in Daphnia sp. Furthermore, a low dietary supply of the ω3-PUFA eicosapentaenoic acid (EPA) has been shown to limit the induction of DVM in Daphnia magna and the performance of D. magna under fluctuating temperatures, as experienced during DVM. In nature DVM of D. magna in response to fish is accompanied by the presence of fish-borne kairomone and diel fluctuations of depth dependent-parameters like temperature, food, and oxygen supply. Here we investigated the effect of factors, which are differing between Daphnia that perform DVM and those which do not. We selected to examine the effect of changing temperature and light conditions and of the presence/absence of fish kairomones on D. magna. For this purpose, we conducted a full factorial experimental design in which we grew D. magna under constantly warm temperatures in a diel light-dark regime or under alternating temperatures in darkness crossed with the presence or absence of fish kairomones. We analyzed the fatty acid composition of mature animals and of their offspring in each treatment. Simulation of the light and temperature regime of migrating animals in presence of the fish kairomone resulted in an increased relative allocation of the ω3-PUFA EPA, from adult animals to their offspring, manifesting as decreased EPA concentrations in mothers and increased EPA concentrations in their offspring in response to simulated DVM (mothers). Additionally, EPA concentrations in the offspring were affected by the interaction of simulated DVM and the fish cue. The presence of the fish kairomone alone increased the EPA concentration in the offspring, that was not experiencing simulated DVM. These findings lead to the conclusion that the temperature and light regime associated with DVM alone, as well as in combination with the DVM-inducing fish kairomones, alter the allocation of fatty acids to the offspring in a manner, which is beneficial for the offspring under the decreased average temperatures, which migrating animals are exposed to. A low dietary supply of ω3-PUFAs may constrain D. magna’s amplitude of DVM, but our results suggest that the next generation of animals may be capable of regaining the full DVM amplitude due to the effect of the fish kairomone and the experienced temperature fluctuations (and darkness) on tissue fatty acid composition. These findings suggest that fatty acid limitation in DVM performing Daphnia may be more severe for the maternal than for the offspring generation.

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Section: Discussionsupporting

confidence: 51%

“…However, we have not assessed membrane fluidity. Only in (Martin-Creuzburg et al, 2019) membrane fluidity and fatty acids have been determined in D. magna. In that study an UI was calculated that was, contrary to the one calculated here, based on fatty acid desaturation related to animal biomass.…”

Section: Discussionmentioning

confidence: 99%

The impact of diel vertical migration on fatty acid patterns and allocation inDaphnia magna

Hahn

Elert

2020

PeerJ

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“…The concentration of EPA within the body was generally much lower than that of the predominant C18 PUFA, 18:3n‐3 and 18:2n‐6, reflecting dietary availability. Assuming that EPA was used as a substitute for C18 PUFA implies that EPA is more efficient in modulating membrane‐related temperature acclimation than C18 PUFA, which has been suggested previously (Martin‐Creuzburg et al., , ).…”

Section: Discussionmentioning

confidence: 70%

“…Instead, animals exposed to the alternating temperatures contained significantly higher amounts of EPA, suggesting that the supplemented EPA was used as a substitute for C18 PUFA (cf. Martin‐Creuzburg et al., ). The concentration of EPA within the body was generally much lower than that of the predominant C18 PUFA, 18:3n‐3 and 18:2n‐6, reflecting dietary availability.…”

Section: Discussionmentioning

confidence: 99%

“…Daphnia have limited capacities to modify the incorporation of dietary PUFA and their body fatty acid profile largely reflects that of their food (Brett, Müller-Navarra, Ballantyne, Ravet, & Goldman, 2006). There is evidence, however, that Daphnia accumulate higher amounts of PUFA within their body when exposed to colder temperatures (Martin-Creuzburg, Coggins, Ebert, & Yampolsky, 2019;Schlechtriem, Arts, & Zellmer, 2006;Zeis, Buchen, Wacker, & Martin-Creuzburg, 2019); whether this also involves a higher degree of fatty acid unsaturation within membrane phospholipids remains unclear. In our experiment, D. magna exposed to alternating temperatures contained higher amounts of C18 PUFA than those exposed to constantly warm temperatures.…”

Section: Daphnia Experiments On the Vertical Migration Behaviour Of mentioning

confidence: 99%

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Dietary polyunsaturated fatty acid supply improves Daphnia performance at fluctuating temperatures, simulating diel vertical migration

et al. 2019

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Diel vertical migration (DVM) is a common predator avoidance strategy of zooplankton. Migration to deeper water layers during the day to escape visually hunting predators is most likely to require physiological adaptations to periodically changing temperatures. Polyunsaturated fatty acids (PUFA) play crucial roles in membrane temperature acclimation. Exposure to cold temperatures typically results in an increase in the relative abundance of PUFA in cell membranes and PUFA requirements of Daphnia increase with decreasing temperatures. To assess the role of dietary PUFA in coping with temperature fluctuations experienced during DVM, we reared Daphnia magna at either constantly warm or fluctuating temperatures, simulating DVM both with and without dietary PUFA supplementation. We show that the well‐known positive effect of dietary eicosapentaenoic acid supplementation on offspring production and population growth rates of D. magna is more pronounced at alternating temperatures than at constantly warm temperatures. Exposure to alternating temperatures caused modification in body PUFA concentrations and, consequently, increased lipid peroxidation. However, detrimental effects of lipid peroxidation were not evident. Our data demonstrate that the capacity to cope with the distinct temperature fluctuations experienced during DVM increases with dietary eicosapentaenoic acid supplementation, suggesting that an adequate dietary PUFA supply is crucial especially for migrating Daphnia populations. A dietary deficiency in long‐chain PUFA may thus severely constrain predator evasion, potentially resulting in increased mortality and cascading effects on lower trophic levels.

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Phenotypic convergence in a natural Daphnia population acclimated to low temperature

Werner

Otte

Elert

2021

Ecology and Evolution

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Fluidity of a given membrane decreases at lower ambient temperatures, whereas it rises at increasing temperatures, which is achieved through changes in membrane lipid composition. In consistence with homeoviscous adaptation theory, lower temperatures result in increased tissue concentrations of polyunsaturated fatty acids (PUFAs) in Daphnia magna, suggesting a higher PUFA requirement at lower temperatures. However, so far homeoviscous adaptation has been suggested for single or geographically separated Daphnia genotypes only. Here, we investigated changes in relative fatty acid (FA) tissue concentrations in response to a lower temperature (15°C) within a D. magna population. We determined juvenile growth rates (JGR) and FA patterns of 14 genotypes that were grown on Chlamydomonas klinobasis at 15°C and 20°C. We report significant differences of JGR and the relative body content of various FAs between genotypes at either temperature and between temperatures. Based on slopes of reaction norms, we found genotype‐specific changes in FA profiles between temperatures suggesting that genotypes have different strategies to cope with changing temperatures. In a hierarchical clustering analysis, we grouped genotypes according to differences in direction and magnitude of changes in relative FA content, which resulted in three clusters of genotypes following different patterns of changes in FA composition. These patterns suggest a lower importance of the PUFA eicosapentaenoic acid (EPA, C20:5ω3) than previously assumed. We calculated an unsaturation index (UI) as a proxy for membrane fluidity at 15°C, and we neither found significant differences for this UI nor for fitness, measured as JGR, between the three genotype clusters. We conclude that these three genotype clusters represent different physiological solutions to temperature changes by altering the relative share of different FAs, but that their phenotypes converge with respect to membrane fluidity and JGR. These clusters will be subjected to different degrees of PUFA limitation when sharing the same diet.

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Rearing Temperature and Fatty Acid Supplementation Jointly Affect Lipid Fluorescence Polarization and Heat Tolerance inDaphnia

Cited by 20 publications

References 40 publications

The impact of diel vertical migration on fatty acid patterns and allocation inDaphnia magna

The impact of diel vertical migration on fatty acid patterns and allocation inDaphnia magna

Dietary polyunsaturated fatty acid supply improves Daphnia performance at fluctuating temperatures, simulating diel vertical migration

Phenotypic convergence in a natural Daphnia population acclimated to low temperature

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