Refine
Year of publication
Language
- English (71)
Is part of the Bibliography
- yes (71) (remove)
Keywords
- food quality (11)
- Daphnia (9)
- zooplankton (7)
- eicosapentaenoic acid (6)
- polyunsaturated fatty acids (6)
- Food quality (5)
- cholesterol (4)
- climate change (4)
- light variability (4)
- phosphorus (4)
Institute
The two important mechanisms influencing the response of phytoplankton communities to alterations of abiotic factors in their environment are difficult to distinguish: species sorting resulting from a change in interspecific competitive pressure, and phenotypic plasticity (here explicitly physiological plasticity i.e. species-specific physiological adjustment). A shift in species composition as well as physiological adjustments in species can lead to changes in fatty acid composition that determine the food quality for zooplankton consumers. We used phytoplankton communities consisting of five species and exposed them to two different light intensities, two light conditions (constant and variable), and two levels of phosphorus supply. Changes in fatty acid and species composition were analyzed. We compared community pairs differing in one factor by calculating the Bray-Curtis similarity index for the composition of both variables. Comparing the Bray-Curtis similarity index of the species composition with the index of the fatty acid composition was used to estimate the effects of species sorting and physiological plasticity. Changes in nutrient supply influenced fatty acid responses based on species sorting and physiological plasticity the most. On one hand, the relevance of physiological plasticity was highest at cultivation in different nutrient supplies but the same light environment. Conversely with low nutrients species sorting appeared to dominate the response to changes in light, while at high nutrients physiological plasticity appeared to influence the response. Overall, under low phosphorus supply the communities showed a lower total fatty acid content per carbon and had increased proportions of saturated and monounsaturated fatty acids. Instead, communities in low light produced more of eicosapentaenoic acid. Our results suggest that the relevance of species sorting and physiological plasticity in shaping the community response highly depends on the environmental factors that influence the system. Nutrient supply had the largest effect, while light had more limited conditional effects. However, all of these factors are important in shaping the food quality of the phytoplankton community for higher trophic levels.
Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.
Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.
In a changing world, phytoplankton communities face a large variety of challenges including altered light regimes. These alterations are caused by more pronounced stratification due to rising temperatures, enhanced eutrophication, and browning of lakes. Community responses toward these effects can emerge as alterations in physiology, biomass, biochemical composition, or diversity. In this study, we addressed the combined effects of changes in light and nutrient conditions on community responses. In particular, we investigated how light intensity and variability under two nutrient conditions influence (1) fast responses such as adjustments in photosynthesis, (2) intermediate responses such as pigment adaptation and (3) slow responses such as changes in community biomass and species composition. Therefore, we exposed communities consisting of five phytoplankton species belonging to different taxonomic groups to two constant and two variable light intensity treatments combined with two levels of phosphorus supply. The tested phytoplankton communities exhibited increased fast reactions of photosynthetic processes to light variability and light intensity. The adjustment of their light harvesting mechanisms via community pigment composition was not affected by light intensity, variability, or nutrient supply. However, pigment specific effects of light intensity, light variability, and nutrient supply on the proportion of the respective pigments were detected. Biomass was positively affected by higher light intensity and nutrient concentrations while the direction of the effect of variability was modulated by light intensity. Light variability had a negative impact on biomass at low, but a positive impact at high light intensity. The effects on community composition were species specific. Generally, the proportion of green algae was higher under high light intensity, whereas the cyanobacterium performed better under low light conditions. In addition to that, the diatom and the cryptophyte performed better with high nutrient supply while the green algae as well as the cyanobacterium performed better at low nutrient conditions. This shows that light intensity, light variability, and nutrient supply interactively affect communities. Furthermore, the responses are highly species and pigment specific, thus to clarify the effects of climate change a deeper understanding of the effects of light variability and species interactions within communities is important.
In a changing world, phytoplankton communities face a large variety of challenges including altered light regimes. These alterations are caused by more pronounced stratification due to rising temperatures, enhanced eutrophication, and browning of lakes. Community responses toward these effects can emerge as alterations in physiology, biomass, biochemical composition, or diversity. In this study, we addressed the combined effects of changes in light and nutrient conditions on community responses. In particular, we investigated how light intensity and variability under two nutrient conditions influence (1) fast responses such as adjustments in photosynthesis, (2) intermediate responses such as pigment adaptation and (3) slow responses such as changes in community biomass and species composition. Therefore, we exposed communities consisting of five phytoplankton species belonging to different taxonomic groups to two constant and two variable light intensity treatments combined with two levels of phosphorus supply. The tested phytoplankton communities exhibited increased fast reactions of photosynthetic processes to light variability and light intensity. The adjustment of their light harvesting mechanisms via community pigment composition was not affected by light intensity, variability, or nutrient supply. However, pigment specific effects of light intensity, light variability, and nutrient supply on the proportion of the respective pigments were detected. Biomass was positively affected by higher light intensity and nutrient concentrations while the direction of the effect of variability was modulated by light intensity. Light variability had a negative impact on biomass at low, but a positive impact at high light intensity. The effects on community composition were species specific. Generally, the proportion of green algae was higher under high light intensity, whereas the cyanobacterium performed better under low light conditions. In addition to that, the diatom and the cryptophyte performed better with high nutrient supply while the green algae as well as the cyanobacterium performed better at low nutrient conditions. This shows that light intensity, light variability, and nutrient supply interactively affect communities. Furthermore, the responses are highly species and pigment specific, thus to clarify the effects of climate change a deeper understanding of the effects of light variability and species interactions within communities is important.
In a changing world, phytoplankton communities face a large variety of challenges including altered light regimes. These alterations are caused by more pronounced stratification due to rising temperatures, enhanced eutrophication, and browning of lakes. Community responses toward these effects can emerge as alterations in physiology, biomass, biochemical composition, or diversity. In this study, we addressed the combined effects of changes in light and nutrient conditions on community responses. In particular, we investigated how light intensity and variability under two nutrient conditions influence (1) fast responses such as adjustments in photosynthesis, (2) intermediate responses such as pigment adaptation and (3) slow responses such as changes in community biomass and species composition. Therefore, we exposed communities consisting of five phytoplankton species belonging to different taxonomic groups to two constant and two variable light intensity treatments combined with two levels of phosphorus supply. The tested phytoplankton communities exhibited increased fast reactions of photosynthetic processes to light variability and light intensity. The adjustment of their light harvesting mechanisms via community pigment composition was not affected by light intensity, variability, or nutrient supply. However, pigment specific effects of light intensity, light variability, and nutrient supply on the proportion of the respective pigments were detected. Biomass was positively affected by higher light intensity and nutrient concentrations while the direction of the effect of variability was modulated by light intensity. Light variability had a negative impact on biomass at low, but a positive impact at high light intensity. The effects on community composition were species specific. Generally, the proportion of green algae was higher under high light intensity, whereas the cyanobacterium performed better under low light conditions. In addition to that, the diatom and the cryptophyte performed better with high nutrient supply while the green algae as well as the cyanobacterium performed better at low nutrient conditions. This shows that light intensity, light variability, and nutrient supply interactively affect communities. Furthermore, the responses are highly species and pigment specific, thus to clarify the effects of climate change a deeper understanding of the effects of light variability and species interactions within communities is important.
Biochemical food quality constraints affect the performance of consumers and mediate trait variation among and within consumer species. To assess inter- and intraspecific differences in fatty acid retention and conversion in freshwater rotifers, we provided four strains of two closely related rotifer species,Brachionus calyciflorussensustricto andBrachionus fernandoi, with food algae differing in their fatty acid composition. The rotifers grazed for 5 days on eitherNannochloropsis limneticaorMonoraphidium minutum, two food algae with distinct polyunsaturated fatty acid (PUFA) profiles, before the diets were switched to PUFA-freeSynechococcus elongatus, which was provided for three more days. We found between- and within-species differences in rotifer fatty acid compositions on the respective food sources and, in particular, highly specific acclimation reactions to the PUFA-free diet. The different reactions indicate inter- but also intraspecific differences in physiological traits, such as PUFA retention, allocation and bioconversion capacities, within the genusBrachionusthat are most likely accompanied by differences in their nutritional demands. Our data suggest that biochemical food quality constraints act differently on traits of closely related species and of strains of a particular species and thus might be involved in shaping ecological interactions and evolutionary processes. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.
Under natural conditions, aboveground herbivory and plant-soil feedbacks (PSFs) are omnipresent interactions strongly affecting individual plant performance. While recent research revealed that aboveground insect herbivory generally impacts the outcome of PSFs, no study tested to what extent the intensity of herbivory affects the outcome. This, however, is essential to estimate the contribution of PSFs to plant performance under natural conditions in the field. Here, we tested PSF effects both with and without exposure to aboveground herbivory for four common grass species in nine grasslands that formed a gradient of aboveground invertebrate herbivory. Without aboveground herbivores, PSFs for each of the four grass species were similar in each of the nine grasslands-both in direction and in magnitude. In the presence of herbivores, however, the PSFs differed from those measured under herbivory exclusion, and depended on the intensity of herbivory. At low levels of herbivory, PSFs were similar in the presence and absence of herbivores, but differed at high herbivory levels. While PSFs without herbivores remained similar along the gradient of herbivory intensity, increasing herbivory intensity mostly resulted in neutral PSFs in the presence of herbivores. This suggests that the relative importance of PSFs for plant-species performance in grassland communities decreases with increasing intensity of herbivory. Hence, PSFs might be more important for plant performance in ecosystems with low herbivore pressure than in ecosystems with large impacts of insect herbivores.
Nitrate or ammonium
(2019)
In freshwaters, algal species are exposed to different inorganic nitrogen (Ni) sources whose incorporation varies in biochemical energy demand. We hypothesized that due to the lesser energy requirement of ammonium (NH4+)-use, in contrast to nitrate (NO3-)-use, more energy remains for other metabolic processes, especially under CO2-and phosphorus (Pi) limiting conditions. Therefore, we tested differences in cell characteristics of the green alga Chlamydomonas acidophila grown on NH4+ or NO3- under covariation of CO2 and Pi-supply in order to determine limitations, in a full-factorial design. As expected, results revealed higher carbon fixation rates for NH4+ grown cells compared to growth with NO3- under low CO2 conditions. NO3- -grown cells accumulated more of the nine analyzed amino acids, especially under Pi-limited conditions, compared to cells provided with NH4+. This is probably due to a slower protein synthesis in cells provided with NO3-. In contrast to our expectations, compared to NH4+ -grown cells NO3- -grown cells had higher photosynthetic efficiency under Pi-limitation. In conclusion, growth on the Ni-source NH4+ did not result in a clearly enhanced Ci-assimilation, as it was highly dependent on Pi and CO2 conditions (replete or limited). Results are potentially connected to the fact that C. acidophila is able to use only CO2 as its inorganic carbon (Ci) source.
Theory predicts that resource variability hinders consumer performance. How this effect depends on the temporal structure of resource fluctuations encountered by individuals remains poorly understood. Combining modelling and growth experiments with Daphnia magna, we decompose the complexity of resource fluctuations and test the effect of resource variance, supply peak timing (i.e. phase) and co-limiting resource covariance along a gradient from high to low frequencies reflecting fine- to coarse-grained environments. Our results show that resource storage can buffer growth at high frequencies, but yields a sensitivity of growth to resource peak timing at lower ones. When two resources covary, negative covariance causes stronger growth depression at low frequencies. However, negative covariance might be beneficial at intermediate frequencies, an effect that can be explained by digestive acclimation. Our study provides a mechanistic basis for understanding how alterations of the environmental grain size affect consumers experiencing variable nutritional quality in nature.
In natural heterogeneous environments, the fitness of animals is strongly influenced by the availability and composition of food. Food quantity and biochemical quality constraints may affect individual traits of consumers differently, mediating fitness response variation within and among species. Using a multifactorial experimental approach, we assessed population growth rate, fecundity, and survival of six strains of the two closely related freshwater rotifer species Brachionus calyciflorus sensu stricto and Brachionus fernandoi. Therefore, rotifers fed low and high concentrations of three algal species differing in their biochemical food quality. Additionally, we explored the potential of a single limiting biochemical nutrient to mediate variations in population growth response. Therefore, rotifers fed a sterol-free alga, which we supplemented with cholesterol-containing liposomes. Co-limitation by food quantity and biochemical food quality resulted in differences in population growth rates among strains, but not between species, although effects on fecundity and survival differed between species. The effect of cholesterol supplementation on population growth was strain-specific but not species-specific. We show that fitness response variations within and among species can be mediated by biochemical food quality. Dietary constraints thus may act as evolutionary drivers on physiological traits of consumers, which may have strong implications for various ecological interactions.
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.
In natural heterogeneous environments, the fitness of animals is strongly influenced by the availability and composition of food. Food quantity and biochemical quality constraints may affect individual traits of consumers differently, mediating fitness response variation within and among species. Using a multifactorial experimental approach, we assessed population growth rate, fecundity, and survival of six strains of the two closely related freshwater rotifer species Brachionus calyciflorus sensu stricto and Brachionus fernandoi. Therefore, rotifers fed low and high concentrations of three algal species differing in their biochemical food quality. Additionally, we explored the potential of a single limiting biochemical nutrient to mediate variations in population growth response. Therefore, rotifers fed a sterol-free alga, which we supplemented with cholesterol-containing liposomes. Co-limitation by food quantity and biochemical food quality resulted in differences in population growth rates among strains, but not between species, although effects on fecundity and survival differed between species. The effect of cholesterol supplementation on population growth was strain-specific but not species-specific. We show that fitness response variations within and among species can be mediated by biochemical food quality. Dietary constraints thus may act as evolutionary drivers on physiological traits of consumers, which may have strong implications for various ecological interactions.
Pharmaceuticals are found in freshwater ecosystems where even low concentrations in the range of ng L−1 may affect aquatic organisms. In the current study, we investigated the effects of chronic exposure to three pharmaceuticals on two microalgae, a potential modulation of the effects by additional inorganic phosphorus (Pi) limitation, and a potential propagation of the pharmaceuticals’ effect across a trophic interaction. The latter considers that pharmaceuticals are bioaccumulated by algae, potentially metabolized into more (or less) toxic derivates and consequently consumed by zooplankton. We cultured Acutodesmus obliquus and Nannochloropsis limnetica in Pi-replete and Pi-limited medium contaminated with one of three commonly human used pharmaceuticals: fluoxetine, ibuprofen, and propranolol. Secondly, we tested to what extent first level consumers (Daphnia magna) were affected when fed with pharmaceutical-grown algae. Chronic exposure, covering 30 generations, led to (i) decreased cell numbers of A. obliquus in the presence of fluoxetine (under Pi-replete conditions) (ii) increased carotenoid to chlorophyll ratios in N. limnetica (under Pi-limited conditions), and (iii) increased photosynthetic yields in A. obliquus (in both Pi-conditions). In addition, ibuprofen affected both algae and their consumer: Feeding ibuprofen-contaminated algae to Pi-stressed D. magna improved their survival. We demonstrate, that even very low concentrations of pharmaceuticals present in freshwater ecosystems can significantly affect aquatic organisms when chronically exposed. Our study indicates that pharmaceutical effects can cross trophic levels and travel up the food chain.
Chemostat experiments are employed to study predator-prey and other trophic interactions, frequently using phytoplankton-zooplankton systems. These experiments often use population dynamics as fingerprints of ecological and evolutionary processes, assuming that the contributions of all major actors to these dynamics are known. However, bacteria are often neglected although they are frequently present. We argue that even without external carbon input bacteria may affect the experimental outcomes depending on experimental conditions and the physiological traits of bacteria, phytoplankton, and zooplankton. Using a static carbon flux model and a dynamic simulation model, we predict the minimum and maximum impact of bacteria on phytoplankton-zooplankton population dynamics. Under bacteria-suppressing conditions, we find that the effect of bacteria is indeed negligible and their omission justified. Under bacteria-favoring conditions, however, bacteria may strongly affect average biomasses of phytoplankton and zooplankton. The population dynamics may become highly complex, which may result in wrong interpretations when inferring processes (e.g., trait changes) from population dynamic patterns without considering bacteria. We provide suggestions to reduce the bacterial impact experimentally. Besides optimizing experimental conditions (e.g., the dilution rate) the appropriate choice of the zooplankton predator is decisive. Counterintuitively, bacteria have a larger impact if the predator is not bacterivorous as high bacterial biomasses and complex population dynamics arise via competition for nutrients with the phytoplankton. Only at least partial bacterivory minimizes the impact of bacteria. Our results help to improve the design of chemostat experiments and their interpretation, and advance the study of ecological and evolutionary processes in aquatic food webs.
Sex-specific differences in nutritional requirements may crucially influence the performances of the sexes, which may have implications for sexual reproduction and thus is of great ecological and evolutionary interest. In the freshwater model species Daphnia magna, essential lipid requirements have been extensively studied. Dietary deficiencies in sterols and polyunsaturated fatty acids (PUFA) have been shown to constrain somatic growth and parthenogenetic reproduction of female Daphnia. In contrast, nutrient requirements of male Daphnia have not been studied yet. Supplementation experiments were conducted to investigate differences in sterol (cholesterol) and PUFA (eicosapentaenoic acid, EPA) requirements between female and male D. magna. Thresholds for sterol-limited juvenile growth were higher in females than in males, suggesting that females are more susceptible to dietary sterol deficiencies than males. Sex-specific differences in maximum somatic growth rates were evident primarily in the presence of dietary EPA; females could not exploit their generally higher growth potential in the absence of dietary PUFA. However, the thresholds for EPA-limited growth did not differ between sexes, suggesting that both sexes have similar dietary EPA requirements during juvenile growth. During a life history experiment, the gain in body dry mass was higher in females than in males, irrespective of food treatment. In both sexes, the gain in body dry mass increased significantly upon EPA supplementation, indicating that both sexes benefited from dietary EPA supply also later in life. However, the positive effects of EPA supplementation were most pronounced for female reproduction-related traits (i.e., clutch sizes, egg dry masses, and total dry mass investment in reproduction). The high maternal investment in reproduction resulted in a depletion of nutrients in female somata. In contrast, the comparatively low paternal investment in reproduction allowed for the accumulation of nutrients in male somata. We conclude that males are generally less susceptible to dietary nutrient deficiencies than females, because they can rely more on internal body stores. Our data suggest that the performances of the sexes are differentially influenced by lipid-mediated food quality, which may have consequences for sexual reproduction and thus the production of resting eggs and the maintenance of Daphnia populations.
Sex-specific differences in nutritional requirements may crucially influence the performances of the sexes, which may have implications for sexual reproduction and thus is of great ecological and evolutionary interest. In the freshwater model species Daphnia magna, essential lipid requirements have been extensively studied. Dietary deficiencies in sterols and polyunsaturated fatty acids (PUFA) have been shown to constrain somatic growth and parthenogenetic reproduction of female Daphnia. In contrast, nutrient requirements of male Daphnia have not been studied yet. Supplementation experiments were conducted to investigate differences in sterol (cholesterol) and PUFA (eicosapentaenoic acid, EPA) requirements between female and male D. magna. Thresholds for sterol-limited juvenile growth were higher in females than in males, suggesting that females are more susceptible to dietary sterol deficiencies than males. Sex-specific differences in maximum somatic growth rates were evident primarily in the presence of dietary EPA; females could not exploit their generally higher growth potential in the absence of dietary PUFA. However, the thresholds for EPA-limited growth did not differ between sexes, suggesting that both sexes have similar dietary EPA requirements during juvenile growth. During a life history experiment, the gain in body dry mass was higher in females than in males, irrespective of food treatment. In both sexes, the gain in body dry mass increased significantly upon EPA supplementation, indicating that both sexes benefited from dietary EPA supply also later in life. However, the positive effects of EPA supplementation were most pronounced for female reproduction-related traits (i.e., clutch sizes, egg dry masses, and total dry mass investment in reproduction). The high maternal investment in reproduction resulted in a depletion of nutrients in female somata. In contrast, the comparatively low paternal investment in reproduction allowed for the accumulation of nutrients in male somata. We conclude that males are generally less susceptible to dietary nutrient deficiencies than females, because they can rely more on internal body stores. Our data suggest that the performances of the sexes are differentially influenced by lipid-mediated food quality, which may have consequences for sexual reproduction and thus the production of resting eggs and the maintenance of Daphnia populations.
Mixing events in stratified lakes result in microalgae being exposed to varying conditions in light and organic carbon concentrations. Stratified lakes consist of an upper illuminated strata and a lower, darker strata where organic carbon accumulates. Therefore, in this contribution we explore the importance of dissolved organic carbon for growth under various light intensities by measuring some ecophysiological adaptations in two green microalgae. We compared the non-motile Chlorella vulgaris with the flagellated Chlamydomonas acidophila under auto-, mixo-, and heterotrophic growth conditions. In both algae the maximum photosynthetic and growth rates were highest under mixotrophy, and both algae appeared inhibited in their phosphorus acquisition under heterotrophy. Heterotrophic conditions provoked the largest differences as C. vulgaris produced chlorophyll a in darkness and grew as well as in autotrophic conditions, whereas Chl. acidophila bleached and could not grow heterotrophically. Although the fatty acid composition of both phytoplankton species differed, both species reacted in a similar way to changes in their growth conditions, mainly by a decrease of C18:3n-3 and an increase of C18:1n-9 from auto- to heterotrophic conditions. The two contrasting responses within the group of green microalgae suggest that dissolved organic carbon has a high deterministic potential to explain the survival and behaviour of green algae in the deeper strata of lakes.
Polyunsaturated fatty acids (PUFA), especially long-chain (i.e., >= 20 carbons) polyunsaturated fatty acids (LC-PUFA), are fundamental to the health and survival of marine and terrestrial organisms. Therefore, it is imperative that we gain a better understanding of their origin, abundance, and transfer between and within these ecosystems. We evaluated the natural variation in PUFA distribution and abundance that exists between and within these ecosystems by amassing and analyzing, using multivariate and analysis of variance (ANOVA) methods, >3000 fatty acid (FA) profiles from marine and terrestrial organisms. There was a clear dichotomy in LC-PUFA abundance between organisms in marine and terrestrial ecosystems, mainly driven by the C-18 PUFA in terrestrial organisms and omega-3 (n-3) LC-PUFA in marine organisms. The PUFA content of an organism depended on both its biome (marine vs terrestrial) and taxonomic group. Within the marine biome, the PUFA content varied among taxonomic groups. PUFA content of marine organisms was dependent on both geographic zone (i.e., latitude, and thus broadly related to temperature) and trophic level (a function of diet). The contents of n-3 LC-PUFA were higher in polar and temperate marine organisms than those from the tropics. Therefore, we conclude that, on a per capita basis, high latitude marine organisms provide a disproportionately large global share of these essential nutrients to consumers, including terrestrial predators. Our analysis also hints at how climate change, and other anthropogenic stressors, might act to negatively impact the global distribution and abundance of n-3 LC-PUFA within marine ecosystems and on the terrestrial consumers that depend on these subsidies.
The mineral and biochemical food quality of prey may limit predator production. This well-studied direct bottom-up effect is especially prominent for herbivore-plant interactions. Low-quality prey species, particularly when defended, are generally considered to be less prone to predator-driven extinction. Undefended high-quality prey species sustain high predator production thereby potentially increasing their own extinction risk. The food quality of primary producers is highly species-specific. In communities of competing prey species, predators thus may supplement their diets of low-quality prey with high-quality prey, leading to indirect horizontal interactions between prey species of different food quality. We explore how these predator-mediated indirect interactions affect species coexistence in a general predator-prey model that is parametrized for an experimental algae-rotifer system. To cover a broad range of three essential functional traits that shape many plant-herbivore interactions we consider differences in 1) the food quality of the prey species, 2) their competitive ability for nutrient uptake and 3) their defence against predation. As expected, low food quality of prey can, similarly to defence, provide protection against extinction by predation. Counterintuitively, our simulations demonstrate that being of high food quality also prevents extinction of that prey species and additionally promotes coexistence with a competing, low-quality prey. The persistence of the high-quality prey enables a high conversion efficiency and control of the low-quality prey by the predator and allows for re-allocation of nutrients to the high-quality competitor. Our results show that high food quality is not necessarily detrimental for a prey species but instead can protect against extinction and promote species richness and functional biodiversity.
Understanding how variance in environmental factors affects physiological performance, population growth, and persistence is central in ecology. Despite recent interest in the effects of variance in single biological drivers, such as temperature, we have lacked a comprehensive framework for predicting how the variances and covariances between multiple environmental factors will affect physiological rates. Here, we integrate current theory on variance effects with co-limitation theory into a single unified conceptual framework that has general applicability. We show how the framework can be applied (1) to generate mathematically tractable predictions of the physiological effects of multiple fluctuating co-limiting factors, (2) to understand how each co-limiting factor contributes to these effects, and (3) to detect mechanisms such as acclimation or physiological stress when they are at play. We show that the statistical covariance of co-limiting factors, which has not been considered before, can be a strong driver of physiological performance in various ecological contexts. Our framework can provide powerful insights on how the global change-induced shifts in multiple environmental factors affect the physiological performance of organisms.
Planktotrons
(2017)
We established a new indoor mesocosm facility, 12 fully controlled Planktotrons, designed to conduct marine and freshwater experiments for biodiversity and food web approaches using natural or artificial, benthic or planktonic communities. The Planktotrons are a unique and custom-tailored facility allowing long-term experiments. Wall growth can be inhibited by a rotating gate paddle with silicone lips. Additionally, temperature and light intensity are individually controllable for each Planktotron and the large volume (600 L) enables high-frequency or volume-intense measurements. In a pilot freshwater experiment various trophic levels of a pelagic food web were maintained for up to 90 d. First, an artificially assembled phytoplankton community of 11 species was inoculated in all Planktotrons. After 22 d, two ciliates were added to all, and three Daphnia species were added to six Planktotrons. After 72 d, dissolved organic matter (DOM, an alkaline soil extract) was added as an external disturbance to six of the 12 Planktotrons, involving three Planktotrons stocked with Daphnia and three without, respectively. We demonstrate the suitability of the Planktotrons for food web and biodiversity research. Variation among replicated Planktotrons (n=3 minimum) did not differ from other laboratory systems and field experiments. We investigated population dynamics and interactions among the different trophic levels, and found them affected by the sequence of ciliate and Daphnia addition and the disturbance caused by addition of DOM.
We studied the short- (12 h) and long-term (144 h) response of Daphnia pulex lipases to quality shifts in diets consisting of different mixtures of the green alga Scenedesmus with the cyanobacterium Synechococcus, two species with contrasting lipid compositions. The lipase/esterase activity in both the gut and the body tissues had fast responses to the diet shift and increased with higher dietary contributions of Synechococcus. When screening the Daphnia genome for TAG lipases, we discovered a large gene-family expansion of these enzymes. We used a subset of eight genes for mRNA expression analyses and distinguished between influences of time and diet on the observed gene expression patterns. We identified five diet-responsive lipases of which three showed a sophisticated short- and long-term pattern of expression in response to small changes in food-quality. Furthermore, the gene expression of one of the lipases was strongly correlated to lipase/esterase activity in the gut suggesting its potentially major role in digestion. These findings demonstrate that the lipid-related enzymatic machinery of D. pulex is finely tuned to diet and might constitute an important mechanism of physiological adaptation in nutritionally complex environments.
The widespread occurrence of melatonin in prokaryotes as well as eukaryotes indicates that this indoleamine is considerably old. This high evolutionary age has led to the development of diverse functions of melatonin in different organisms, such as the detoxification of reactive oxygen species and anti-stress effects. In insects, i.e. Drosophila, the addition of melatonin has also been shown to increase the life span of this arthropod, probably by reducing age-related increasing oxidative stress.
Although the presence of melatonin was recently found to exist in the ecological and toxicological model organism Daphnia, its function in this cladoceran has thus far not been addressed. Therefore, we challenged Daphnia with three different stressors in order to investigate potential stress-response attenuating effects of melatonin. i) Female and male daphnids were exposed to melatonin in a longevity experiment, ii) Daphnia were confronted with stress signals from the invertebrate predator Chaoborus sp., and iii) Daphnia were grown in high densities, i.e. under crowding-stress conditions.
Results
In our experiments we were able to show that longevity of daphnids was not affected by melatonin. Therefore, age-related increasing oxidative stress was probably not compensated by added melatonin. However, melatonin significantly attenuated Daphnia’ s response to acute predator stress, i.e. the formation of neckteeth which decrease the ability of the gape-limited predator Chaoborus sp. to handle their prey. In addition, melatonin decreased the extent of crowding-related production of resting eggs of Daphnia.
Conclusions
Our results confirm the effect of melatonin on inhibition of stress-signal responses of Daphnia. Until now, only a single study demonstrated melatonin effects on behavioral responses due to vertebrate kairomones, whereas we clearly show a more general effect of melatonin: i) on morphological predator defense induced by an invertebrate kairomone and ii) on life history characteristics transmitted by chemical cues from conspecifics. Therefore, we could generally confirm that melatonin plays a role in the attenuation of responses to different stressors in Daphnia.
We studied the short- (12 h) and long-term (144 h) response of Daphnia pulex lipases to quality shifts in diets consisting of different mixtures of the green alga Scenedesmus with the cyanobacterium Synechococcus, two species with contrasting lipid compositions. The lipase/esterase activity in both the gut and the body tissues had fast responses to the diet shift and increased with higher dietary contributions of Synechococcus. When screening the Daphnia genome for TAG lipases, we discovered a large gene-family expansion of these enzymes. We used a subset of eight genes for mRNA expression analyses and distinguished between influences of time and diet on the observed gene expression patterns. We identified five diet-responsive lipases of which three showed a sophisticated short- and long-term pattern of expression in response to small changes in food-quality. Furthermore, the gene expression of one of the lipases was strongly correlated to lipase/esterase activity in the gut suggesting its potentially major role in digestion. These findings demonstrate that the lipid-related enzymatic machinery of D. pulex is finely tuned to diet and might constitute an important mechanism of physiological adaptation in nutritionally complex environments.
Linking primary producer diversity and food quality effects on herbivores: A biochemical perspective
(2017)
Biodiversity can strongly influence trophic interactions. The nutritional quality of prey communities and how it is related to the prey diversity is suspected to be a major driver of biodiversity effects. As consumer growth can be co-limited by the supply of several biochemical components, biochemically diverse prey communities should promote consumer growth. Yet, there is no clear consensus on how prey specific diversity is linked to community biochemical diversity since previous studies have considered only single nutritional quality traits. Here, we demonstrate that phytoplankton biochemical traits (fatty acids and sterols) can to a large extent explain Daphnia magna growth and its apparent dependence on phytoplankton species diversity. We find strong correlative evidence between phytoplankton species diversity, biochemical diversity, and growth. The relationship between species diversity and growth was partially explained by the fact that in many communities Daphnia was co-limited by long chained polyunsaturated fatty acids and sterols, which was driven by different prey taxa. We suggest that biochemical diversity is a good proxy for the presence of high food quality taxa, and a careful consideration of the distribution of the different biochemical traits among species is necessary before concluding about causal links between species diversity and consumer performance.
We tested the influence of two light intensities [40 and 300 μmol PAR / (m2s)] on the fatty acid composition of three distinct lipid classes in four freshwater phytoplankton species. We chose species of different taxonomic classes in order to detect potentially similar reaction characteristics that might also be present in natural phytoplankton communities. From samples of the bacillariophyte Asterionella formosa, the chrysophyte Chromulina sp., the cryptophyte Cryptomonas ovata and the zygnematophyte Cosmarium botrytis we first separated glycolipids (monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and sulfoquinovosyldiacylglycerol), phospholipids (phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, phosphatidylinositol, and phosphatidylserine) as well as non-polar lipids (triacylglycerols), before analyzing the fatty acid composition of each lipid class. High variation in the fatty acid composition existed among different species. Individual fatty acid compositions differed in their reaction to changing light intensities in the four species. Although no generalizations could be made for species across taxonomic classes, individual species showed clear but small responses in their ecologically-relevant omega-3 and omega-6 polyunsaturated fatty acids (PUFA) in terms of proportions and of per tissue carbon quotas. Knowledge on how lipids like fatty acids change with environmental or culture conditions is of great interest in ecological food web studies, aquaculture, and biotechnology, since algal lipids are the most important sources of omega-3 long-chain PUFA for aquatic and terrestrial consumers, including humans.
Organism growth can be limited either by a single resource or by multiple resources simultaneously (co-limitation). Efforts to characterise co-limitation have generated two influential approaches. One approach uses limitation scenarios of factorial growth assays to distinguish specific types of co-limitation; the other uses growth responses spanned over a continuous, multi-dimensional resource space to characterise different types of response surfaces. Both approaches have been useful in investigating particular aspects of co-limitation, but a synthesis is needed to stimulate development of this recent research area. We address this gap by integrating the two approaches, thereby presenting a more general framework of co-limitation. We found that various factorial (co-)limitation scenarios can emerge in different response surface types based on continuous availabilities of essential or substitutable resources. We tested our conceptual co-limitation framework on data sets of published and unpublished studies examining the limitation of two herbivorous consumers in a two-dimensional resource space. The experimental data corroborate the predictions, suggesting a general applicability of our co-limitation framework to generalist consumers and potentially also to other organisms. The presented framework might give insight into mechanisms that underlie co-limitation responses and thus can be a seminal starting point for evaluating co-limitation patterns in experiments and nature.
Understanding animal performance in heterogeneous or variable environments is a central question in ecology. We combine modelling and experiments to test how temperature and food availability variance jointly affect life-history traits of ectotherms. The model predicts that as mean temperatures move away from the ectotherm's thermal optimum, the effect size of joint thermal and food variance should become increasingly sensitive to their covariance. Below the thermal optimum, performance should be positively correlated with food–temperature covariance and the opposite is predicted above it. At lower temperatures, covariance should determine whether food and temperature variance increases or decreases performance compared to constant conditions. Somewhat stronger than predicted, the covariance effect below the thermal optimum was confirmed experimentally on an aquatic ectotherm (Daphnia magna) exposed to diurnal food and temperature variance with different amounts of covariance. Our findings have important implications for understanding ectotherm responses to climate-driven alterations of thermal mean and variance.
We tested the influence of two light intensities [40 and 300 μmol PAR / (m2s)] on the fatty acid composition of three distinct lipid classes in four freshwater phytoplankton species. We chose species of different taxonomic classes in order to detect potentially similar reaction characteristics that might also be present in natural phytoplankton communities. From samples of the bacillariophyte Asterionella formosa, the chrysophyte Chromulina sp., the cryptophyte Cryptomonas ovata and the zygnematophyte Cosmarium botrytis we first separated glycolipids (monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and sulfoquinovosyldiacylglycerol), phospholipids (phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, phosphatidylinositol, and phosphatidylserine) as well as non-polar lipids (triacylglycerols), before analyzing the fatty acid composition of each lipid class. High variation in the fatty acid composition existed among different species. Individual fatty acid compositions differed in their reaction to changing light intensities in the four species. Although no generalizations could be made for species across taxonomic classes, individual species showed clear but small responses in their ecologically-relevant omega-3 and omega-6 polyunsaturated fatty acids (PUFA) in terms of proportions and of per tissue carbon quotas. Knowledge on how lipids like fatty acids change with environmental or culture conditions is of great interest in ecological food web studies, aquaculture, and biotechnology, since algal lipids are the most important sources of omega-3 long-chain PUFA for aquatic and terrestrial consumers, including humans.
Recently pharmaceuticals have become significant environmental pollutants in aquatic ecosystems, that could affect primary producers such as microalgae. Here we analyzed the effect of pharmaceuticals on the photosynthesis of microalgae commonly found in freshwater-two species of Chlorophyceae and a member of the Eustigmatophyceae, via PAM fluorometry. As pharmaceuticals, three medicines often consumed in households were chosen: (i) fluoxetine, an antidepressant, (ii) propranolol, a beta-blocker and (iii) ibuprofen, an anti-inflammatory and analgesic medicine. The EC50 for the quantum yield of photosystem II in phytoplankton acclimated to inorganic phosphorus (P-i)-replete and P-i-limited conditions was estimated. Acute toxicity experiments over a 5 h exposure revealed that Nannochloropsis limnetica was the least sensitive to pharmaceuticals in its photosynthetic yield out of all species tested. Although the estimation of sub-lethal effects can be vital in contrast to that of LC(50)s, the EC50 values in all species and for all medicines were orders of magnitude higher than concentrations found in polluted surface water. Chlamydomonas reinhardtii was the most sensitive to fluoxetine (EC50 of 1.6 mg L-1), and propranolol (EC50 of 3 mg L-1). Acutodesmus obliquus was most sensitive to ibuprofen (EC50 of 288 mg L-1). Additionally, the sensitivity to the pharmaceuticals changed under a P-i-limitation; the green algae became less sensitive to fluoxetine and propranolol. In contrast, P-i-limited algal species were more sensitive to ibuprofen. Our results suggest that the sensitivity of algae to pharmaceuticals is (i) highly compound- and species-specific and (ii) dependent on the cellular P status.
Photosynthetic acclimation of phytoplankton to lower irradiation can be met by several strategies such as increasing the affinity for light or increasing antenna size and stacking of the thylakoids. The latter is reflected by a higher proportion of polyunsaturated fatty acids (PUFAs). Additionally, photosynthetic capacity (P-max), respiratory losses, and proton leakage can be reduced under low light. Here we consider the effect of light intensity and phosphorus availability simultaneously on the photosynthetic acclimation and fatty acid composition of four phytoplankters. We studied representatives of the Chlorophyceae, Cryptophyceae and Mediophyceae, all of which are important components of plankton communities in temperate lakes. In our analysis, excluding fatty acid composition, we found different acclimation strategies in the chlorophytes Scenedesmus quadricauda, Chlamydomonas globosa, cryptophyte Cryptomonas ovata and ochrophyte Cyclotella meneghiniana. We observed interactive effects of light and phosphorus conditions on photosynthetic capacity in S. quadricauda and Cry. ovata. Cry. ovata can be characterized as a low light-acclimated species, whereas S. quadricauda and Cyc. meneghiniana can cope best with a combination of high light intensities and low phosphorus supply. Principal component analyses (PCA), including fatty acid composition, showed further species-specific patterns in their regulation of P-max with PUFAs and light. In S. quadricauda and Cyc. meneghiniana, PUFAs negatively affected the relationship between P-max and light. In Chl. globosa, lower light coincided with higher PUFAs and lower P-max, but PCA also indicated that PUFAs had no direct influence on P-max. PUFAs and P-max were unaffected by light in Cry. ovata. We did not observe a general trend in the four species tested and concluded that, in particular, the interactive effects highlight the importance of taking into account more than one environmental factor when assessing photosynthetic acclimation to lower irradiation.
Long-chain polyunsaturated fatty acids (LC-PUFA) are critical for the health of aquatic and terrestrial organisms; therefore, understanding the production, distribution, and abundance of these compounds is imperative. Although the dynamics of LC-PUFA production and distribution in aquatic environments has been well documented, a systematic and comprehensive comparison to LC-PUFA in terrestrial environments has not been rigorously investigated. Here we use a data synthesis approach to compare and contrast fatty acid profiles of 369 aquatic and terrestrial organisms. Habitat and trophic level were interacting factors that determined the proportion of individual omega-3 (n-3) or omega-6 (n-6) PUFA in aquatic and terrestrial organisms. Higher total n-3 content compared with n-6 PUFA and a strong prevalence of the n-3 PUFA eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) characterized aquatic versus terrestrial organisms. Conversely, terrestrial organisms had higher linoleic acid (LNA) and alpha-linolenic acid (ALA) contents than aquatic organisms; however, the ratio of ALA: LNA was higher in aquatic organisms. The EPA + DHA content was higher in aquatic animals than terrestrial organisms, and increased from algae to invertebrates to vertebrates in the aquatic environment. An analysis of covariance (ANCOVA) revealed that fatty acid composition was highly dependent on the interaction between habitat and trophic level. We conclude that freshwater ecosystems provide an essential service through the production of n-3 LC-PUFA that are required to maintain the health of terrestrial organisms including humans.
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 omega 3 PUFAs alpha-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.
The underlying mechanisms and consequences of competition and diversity are central themes in ecology. A higher diversity of primary producers often results in higher resource use efficiency in aquatic and terrestrial ecosystems. This may result in more food for consumers on one hand, while, on the other hand, it can also result in a decreased food quality for consumers; higher biomass combined with the same availability of the limiting compound directly reduces the dietary proportion of the limiting compound. Here we tested whether and how interspecific competition in phytoplankton communities leads to changes in resource use efficiency and cellular concentrations of nutrients and fatty acids. The measured particulate carbon : phosphorus ratios (C:P) and fatty acid concentrations in the communities were compared to the theoretically expected ratios and concentrations of measurements on simultaneously running monocultures. With interspecific competition, phytoplankton communities had higher concentrations of the monounsaturated fatty acid oleic acid and also much higher concentrations of the ecologically and physiologically relevant long-chain polyunsaturated fatty acid eicosapentaenoic acid than expected concentrations based on monocultures. Such higher availability of essential fatty acids may contribute to the positive relationship between phytoplankton diversity and zooplankton growth, and may compensate limitations by mineral nutrients in higher trophic levels.
In freshwater systems, Daphnia has been demonstrated to show adaptive responses following the light-dark cycle. The adjustment of these responses to the change of day and night is probably transmitted via the hormone melatonin. The rate-limiting enzyme in melatonin synthesis is the arylalkylamine N-transferase (AANAT). We identified three genes coding for insect-like AANATs in Daphnia, of which we measured the gene expression in an ecologically relevant light-dark cycle. We demonstrated that Daphnia's insect-like AANAT gene expression oscillated in a daily manner, and that the highest peak of expression after the onset of darkness was followed by a peak of melatonin production at midnight. Moreover, we could show an oscillation of endogenous melatonin synthesis in Daphnia. In most organisms, melatonin synthesis is due to rhythmic expression of genes of the circadian clock, since transcription of aanats is directly linked to a circadian transcription factor. We could demonstrate that putative clock genes and insect-like AANAT genes of Daphnia were equally expressed. Therefore, we propose that melatonin synthesis is coupled to the expression of Daphnia clock genes, and that insect-like AANATs of crustaceans have a similar function as AANATs of vertebrates: The initiation of melatonin synthesis. In future studies with Daphnia, it will be necessary to take the time of day into account since melatonin concentrations might influence stress responses.
In this pilot study, we describe a high-pressure incubation system allowing multiple subsampling of a pressurized culture without decompression. The system was tested using one piezophilic (Photobacterium profundum), one piezotolerant (Colwellia maris) bacterial strain and a decompressed sample from the Mediterranean deep sea (3044 m) determining bacterial community composition, protein production (BPP) and cell multiplication rates (BCM) up to 27 MPa. The results showed elevation of BPP at high pressure was by a factor of 1.5 +/- 1.4 and 3.9 +/- 2.3 for P. profundum and C. maris, respectively, compared to ambient-pressure treatments and by a factor of 6.9 +/- 3.8 fold in the field samples. In P. profundum and C. maris, BCM at high pressure was elevated (3.1 +/- 1.5 and 2.9 +/- 1.7 fold, respectively) compared to the ambient-pressure treatments. After 3 days of incubation at 27 MPa, the natural bacterial deep-sea community was dominated by one phylum of the genus Exiguobacterium, indicating the rapid selection of piezotolerant bacteria. In future studies, our novel incubation system could be part of an isopiestic pressure chain, allowing more accurate measurement of bacterial activity rates which is important both for modeling and for predicting the efficiency of the oceanic carbon pump.
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.
Daphnia's dilemma: adjustment of carbon budgets in the face of food and cholesterol limitation
(2014)
We studied the carbon (C) metabolism in Daphnia when the amount of C (food quantity) and/or the content of biochemical nutrients (food quality) was limiting. Growth performances and C budgets of Daphnia magna (assimilation, faeces egestion, excretion and respiration measured by [C-14]-tracing) were analysed when animals were raised on different food quantities and concentrations of cholesterol, an essential biochemical food compound. Cholesterol is of special interest because it not only acts as limiting nutrient but also contributes to the overall C pool of the animals. As the tissue cholesterol concentration in Daphnia is quite low, we hypothesized the selective exclusion of cholesterol from C budgeting and tested this using radiolabelled cholesterol. Somatic growth rates of D. magna were highest at high quantity and quality and were reduced to a moderate value if either the food quantity or the cholesterol concentration was low. Growth was lowest at low food quantity and quality. The measurements of C budgets revealed high regulative response to low food quality at high food quantity only. Here, low dietary cholesterol caused bulk C assimilation efficiency (AE) to decrease and assimilated (excess) C to be increasingly respired. Additionally, Daphnia enhanced efficient adjustment of C budgets when facing cholesterol limitation by (1) increasing the AE of the cholesterol itself and (2) not changing cholesterol respiration, which was still not detectable. In contrast, at low food quantity, Daphnia is unable to adjust for low food quality, emphasizing that food limitation could overrule food quality effects.
Daphnia responds to low availability of carbon (food quantity) or limiting concentrations of nutrients relative to carbon (C) in excess (food quality) by respectively saving or discharging C via different pathways. We investigated which kind of food limitation leads to a faster regulation in Daphnia C budgets, and whether the pre-assimilative C pathways, ingestion and faeces egestion and the post-assimilative C pathways, excretion and respiration, are regulated concurrently. Daphnia magna were exposed to dietary shifts in different food quantities or qualities; food quality was varied in terms of the essential component, cholesterol. After acclimation to the new diet ranging from 0 to 96 h, C budgets were measured by a radiotracer technique. Dietary shifts in quantity and quality caused Daphnia to quickly adjust their C budgets within 6 h, but different C pathways were affected. A shift to low food quantity reduced Daphnia respiration indicating C retention. In contrast, sudden low quality food caused increased faeces egestion to discharge excess C. Furthermore, we observed a delayed increase in excretion but no change in respiration within the time frame studied. Such time-shifted responses appear to be an appropriate means to keep the costs of physiological adjustments relatively low, which in turn would benefit Daphnia performance.
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 mu g mg C-1) and encompass the one for cholesterol (8.9 mu g 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.
The neonate nutrition hypothesis - early feeding affects the body stoichiometry of Daphnia offspring
(2013)
Aquatic herbivores consume variable quantities and qualities of food. In freshwater systems, where phosphorus (P) is often a primary limiting element, inadequate dietary P can slow maternal growth and reduce body P content. There remains uncertainty about whether and how dietary effects on mothers are transferred to offspring by way of egg provisioning. Using the keystone herbivore Daphnia, we tested a novel explanation (the neonate nutrition hypothesis') to determine whether the early nutrition of newborns affects their elemental composition and whether the indications of differences in maternal P nutrition found previously might be overestimated. We thus examined the P content of mothers and their eggs from deposition through development to the birth of neonates. We examined further whether very short periods of ingestion (3h) by the offspring alter the overall P content of juvenile Daphnia. We showed that strong dietary P effects on mothers were not directly transferred to their eggs. Irrespective of the supply of P in the maternal diet, the P content of eggs in different developmental stages and in (unfed) neonates did not differ. This indicates that Daphnia mothers do not reduce the quality (in terms of P) of newly produced offspring after intermittent periods (i.e. several days) of poor nutrition. In contrast, the P content of neonates reflected that of their food after brief periods of feeding, indicating that even temporary exposure to nutrient poor food immediately after birth may strongly affect the elemental composition of neonates. Our results thus support the neonate nutrition hypothesis, which, like differential maternal provisioning, is a possible explanation for the variable elemental quality of young Daphnia.
The nutrition of animal consumers is an important regulator of ecological processes due to its effects on their physiology, life-history and behaviour. Understanding the ecological effects of poor nutrition depends on correctly diagnosing the nature and strength of nutritional limitation. Despite the need to assess nutritional limitation, current approaches to delineating nutritional constraints can be non-specific and imprecise. Here, we consider the need and potential to develop new complementary approaches to the study of nutritional constraints on animal consumers by studying and using a suite of established and emerging biochemical and molecular responses. These nutritional indicators include gene expression, transcript regulators, protein profiling and activity, and gross biochemical and elemental composition. The potential applications of nutritional indicators to ecological studies are highlighted to demonstrate the value that this approach would have to future studies in community and ecosystem ecology.
In aquatic food webs, consumers, such as daphnids and copepods, differ regarding their accumulation of polyunsaturated fatty acids (PUFAs). We tested if the accumulation of PUFAs in a seston size fraction containing different consumers and in Daphnia as a separate consumer is subject to seasonal changes in a large deep lake due to changes in the dietary PUFA supply and specific demands of different consumers. We found that the accumulation of arachidonic acid (ARA) in Daphnia increased from early summer to late summer and autumn. However, ARA requirements of Daphnia appeared to be constant throughout the year, because the accumulation of ARA increased when the dietary ARA supply decreased. In the size fraction 140 m, we found an increased accumulation of docosahexaenoic acid (DHA) during late summer and autumn. These seasonal changes in DHA accumulation were linked to changes in the proportion of copepods in this size fraction, which may have increasingly accumulated DHA for active overwintering. We show that consumer-specific PUFA demands can result in seasonal changes in PUFA accumulation, which may influence the trophic transfer of PUFAs within the food web.
1. The polyunsaturated fatty acid eicosapentaenoic acid (EPA) plays an important role in aquatic food webs, in particular at the primary producerconsumer interface where keystone species such as daphnids may be constrained by its dietary availability. Such constraints and their seasonal and interannual changes may be detected by continuous measurements of EPA concentrations. However, such EPA measurements became common only during the last two decades, whereas long-term data sets on plankton biomass are available for many well-studied lakes. Here, we test whether it is possible to estimate EPA concentrations from abiotic variables (light and temperature) and the biomass of prey organisms (e.g. ciliates, diatoms and cryptophytes) that potentially provide EPA for consumers. 2. We used multiple linear regression to relate size- and taxonomically resolved plankton biomass data and measurements of temperature and light intensity to directly measured EPA concentrations in Lake Constance during a whole year. First, we tested the predictability of EPA concentrations from the biomass of EPA-rich organisms (diatoms, cryptophytes and ciliates). Secondly, we included the variables mean temperature and mean light intensity over the sampling depth (020 m) and depth (08 and 820 m) as factors in our model to check for large-scale seasonal- and depth-dependent effects on EPA concentrations. In a third step, we included the deviations of light and temperature from mean values in our model to allow for their potential influence on the biochemical composition of plankton organisms. We used the Akaike Information Criterion to determine the best models. 3. All approaches supported our proposition that the biomasses of specific plankton groups are variables from which seston EPA concentrations can be derived. The importance of ciliates as an EPA source in the seston was emphasised by their high weight in our models, although ciliates are neglected in most studies that link fatty acids to seston taxonomic composition. The large-scale seasonal variability of light intensity and its interaction with diatom biomass were significant predictors of EPA concentrations. The deviation of temperature from mean values, accounting for a depth-dependent effect on EPA concentrations, and its interaction with ciliate biomass were also variables with high predictive power. 4. The best models from the first and second approaches were validated with measurements of EPA concentrations from another year (1997). The estimation with the best model including only biomass explained 80%, and the best model from the second approach including mean temperature and depth explained 87% of the variability in EPA concentrations in 1997. 5. We show that it is possible to predict EPA concentrations reliably from plankton biomass, while the inclusion of abiotic factors led to results that were only partly consistent with expectations from laboratory studies. Our approach of including biotic predictors should be transferable to other systems and allow checking for biochemical constraints on primary consumers.
1. Poikilothermic animals incorporate more polyunsaturated fatty acids (PUFAs) into their cellular membranes as temperature declines, suggesting an increased sensitivity to PUFA limitation in cool conditions. To test this we raised Daphnia magna at different temperatures and investigated the effect of varying dietary PUFA on life history parameters (i.e. growth, reproduction) and the PUFA composition of body tissue and eggs.
2. Upon a PUFA-rich diet (Cryptomonas sp.) females showed higher concentrations of several omega 3 PUFAs in their body tissue at 15 degrees C than at 20 degrees C and 25 degrees C, indicating a greater structural requirement for omega 3 PUFAs at low temperature. Their eggs had an equal but higher concentration of omega 3 PUFAs than their body tissue.
3. In a life history experiment at 15 and 20 degrees C we supplemented a diet of a PUFA-free cyanobacterium with the omega 3 PUFA eicosapentaenoic acid (EPA). The growth of D. magna was more strongly EPA limited at low temperature. A greater requirement for structural EPA at 15 degrees C was indicated by a steeper increase in somatic EPA content with dietary EPA compared to 20 degrees C.
4. At 20 degrees C the development of eggs to successful hatching was high when EPA was supplied to the mothers. At 15 degrees C the hatching success was generally poor, despite of a higher maternal provision of EPA to eggs, compared to that at 20 degrees C, suggesting that EPA alone was insufficient for proper neonatal development at the low temperature. The growth of offspring from mothers raised at 20 degrees C without EPA supplementation was very low, indicating that the negative effects of EPA deficiency can be carried on to the next generation.
5. The fatty acid composition of Daphnia sp. in published field studies shows increasing proportions of saturated fatty acids with increasing environmental temperature, whereas omega 3 PUFAs and EPA show no clear pattern, suggesting that variations in dietary PUFA may mask temperature-dependent adjustments in omega 3 PUFA concentrations of cladocerans in nature.
We tested, in the laboratory, the influence of light intensity, temperature, and phosphorus (P) supply on fatty acid (FA) concentrations of four freshwater algae: the green algae Scenedesmus quadricauda (Turpin) Breb. and Chlamydomonas globosa J. Snow, the cryptophyte Cryptomonas ovata Ehrenb., and the diatom Cyclotella meneghiniana Kutz. We investigated the main and interactive effects of two variables on algal FA concentrations (i.e., light intensity and P supply or temperature and P supply). Interactive effects of light intensity and P supply were most pronounced in C. meneghiniana, but were also found in S. quadricauda and C. ovata. Changes in several saturated and unsaturated FA concentrations with light were more distinct in the low-P treatments than in the high-P treatments. Interactive effects of temperature and P supply on various FA concentrations were observed in all four species, but there was no consistent pattern. In lake ecosystems, P limitation often coincides with high light intensities and temperatures in summer. Therefore, it is important to examine how combinations of these environmental conditions affect FA concentrations of primary producers that are important sources of FAs for higher trophic levels.
Red, orange or green snow is the macroscopic phenomenon comprising different eukaryotic algae. Little is known about the ecology and nutrient regimes in these algal communities. Therefore, eight snow algal communities from five intensively tinted snow fields in western Spitsbergen were analysed for nutrient concentrations and fatty acid (FA) composition. To evaluate the importance of a shift from green to red forms on the FA-variability of the field samples, four snow algal strains were grown under nitrogen replete and moderate light (+N+ML) or N-limited and high light (-N+HL) conditions. All eight field algal communities were dominated by red and orange cysts. Dissolved nutrient concentration of the snow revealed a broad range of NH4+ (<0.005-1.2 mg NI-1) and only low PO43- (< 18 mu g P I-1) levels. The external nutrient concentration did not reflect cellular nutrient ratios as C:N and C:P ratios of the communities were highest at locations containing relatively high concentrations of NH4- and PO43-. Molar N:P ratios ranged from 11 to 21 and did not suggest clear limitation of a single nutrient. On a per carbon basis, we found a 6-fold difference in total FA content between the eight snow algal communities, ranging from 50 to 300 mg FA g C-1. In multivariate analyses total FA content opposed the cellular N:C quota and a large part of the FA variability among field locations originated from the abundant FAs C181n-9, C18 2n-6, and C183n-3. Both field samples and snow algal strains grown under -N+HL conditions had high concentrations of C181n-9. FAs possibly accumulated due to the cessation of growth. Differences in color and nutritional composition between patches of snow algal communities within one snow field were not directly related to nutrient conditions. We propose that the highly patchy distribution of snow algae within and between snow fields may also result from differences in topographical and geological parameters such as slope, melting water rivulets, and rock formation.
To assess nutritional consequences associated with lake oligotrophication for aquatic consumers, we analyzed the elemental and biochemical composition of natural seston and concomitantly conducted laboratory growth experiments in which the freshwater key herbivore Daphnia was raised on natural seston of the nowadays (2008) oligotrophic Lake Constance throughout an annual cycle. Food quality mediated constraints on Daphnia performance were assessed by comparing somatic growth rates with seston characteristics (multiple regression analysis) and by manipulating the elemental and biochemical composition of natural seston experimentally (nutrient supplementation). Results were compared to similar experiments carried out previously (1997) during a mesotrophic phase of the lake. In the oligotrophic phase, particulate carbon and phosphorus concentrations were lower, fatty acid concentrations were higher, and the taxonomic composition of phytoplankton was less diverse, with a more diatom- and cryptophytes-dominated community, compared to the previous mesotrophic phase. Multiple regression analysis indicated a shift from a simultaneous limitation by food quantity (in terms of carbon) and quality (i.e. a-linolenic acid) during the mesotrophic phase to a complex multiple nutrient limitation mediated by food quantity, phosphorus, and omega-3 fatty acids in the following oligotrophic phase. The concomitant supplementation experiments also revealed seasonal changes in multiple resource limitations, i.e. the prevalent limitation by food quantity was accompanied by a simultaneous limitation by either phosphorus or omega-3 fatty acids, and thus confirmed and complemented the multiple regression approach. Our results indicate that seasonal and annual changes in nutrient availabilities can create complex co-limitation scenarios consumers have to cope with, which consequently may also affect the efficiency of energy transfer in food webs.
It has been proposed that growth and reproduction of animals is frequently limited by multiple nutrients simultaneously. To improve our understanding of the consequences of multiple nutrient limitations (i.e. co-limitation) for the performance of animals, we conducted standardized population growth experiments using an important aquatic consumer, the rotifer Brachionus calyciflorus. We compared nutrient profiles (sterols, fatty acids and amino acids) of rotifers and their diets to reveal consumerdiet imbalances and thus potentially limiting nutrients. In concomitant growth experiments, we directly supplemented potentially limiting substances (sterols, fatty acids, amino acids) to a nutrient-deficient diet, the cyanobacterium Synechococcus elongatus, and recorded population growth rates. The results from the supplementation experiments corroborated the nutrient limitations predicted by assessing consumerdiet imbalances, but provided more detailed information on co-limiting nutrients. While the fatty acid deficiency of the cyanobacterium appeared to be of minor importance, the addition of both cholesterol and certain amino acids (leucine and isoleucine) improved population growth rates of rotifers, indicating a simultaneous limitation by sterols and amino acids. Our results add to growing evidence that consumers frequently face multiple nutrient limitations and suggest that the concept of co-limitation has to be considered in studies assessing nutrient-limited growth responses of consumers.