Photosynthetic activity in both algae and cyanobacteria changes in response to cues of predation
(2022)
A plethora of adaptive responses to predation has been described in microscopic aquatic producers.
Although the energetic costs of these responses are expected, with their consequences going far beyond an individual, their underlying molecular and metabolic mechanisms are not fully known.
One, so far hardly considered, is if and how the photosynthetic efficiency of phytoplankton might change in response to the predation cues. Our main aim was to identify such responses in phytoplankton and to detect if they are taxon-specific.
We exposed seven algae and seven cyanobacteria species to the chemical cues of an efficient consumer, Daphnia magna, which was fed either a green alga, Acutodesmus obliquus, or a cyanobacterium, Synechococcus elongatus (kairomone and alarm cues), or was not fed (kairomone alone).
In most algal and cyanobacterial species studied, the quantum yield of photosystem II increased in response to predator fed cyanobacterium, whereas in most of these species the yield did not change in response to predator fed alga.
Also, cyanobacteria tended not to respond to a non-feeding predator. The modal qualitative responses of the electron transport rate were similar to those of the quantum yield.
To our best knowledge, the results presented here are the broadest scan of photosystem II responses in the predation context so far.
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.
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.
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.
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.
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.
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.
For the ecological risk assessment of toxic chemicals, standardized tests on individuals are often used as proxies for population-level effects. Here, we address the utility of one commonly used metric, reproductive output, as a proxy for population-level effects. Because reproduction integrates the outcome of many interacting processes (e.g., feeding, growth, allocation of energy to reproduction), the observed toxic effects in a reproduction test could be due to stress on one of many processes. Although this makes reproduction a robust endpoint for detecting stress, it may mask important population-level consequences if the different physiological processes stress affects are associated with different feedback mechanisms at the population level. We therefore evaluated how an observed reduction in reproduction found in a standard reproduction test translates to effects at the population level if it is caused by hypothetical toxicants affecting different physiological processes (physiological modes of action; PMoA). For this we used two consumer-resource models: the Yodzis-Innes (YI) model, which is mathematically tractable, but requires strong assumptions of energetic equivalence among individuals as they progress through ontogeny, and an individual-based implementation of dynamic energy budget theory (DEB-IBM), which relaxes these assumptions at the expense of tractability. We identified two important feedback mechanisms controlling the link between individual- and population-level stress in the YI model. These mechanisms turned out to also be important for interpreting some of the individual-based model results; for two PMoAs, they determined the population response to stress in both models. In contrast, others stress types involved more complex feedbacks, because they asymmetrically stressed the production efficiency of reproduction and somatic growth. The feedbacks associated with different PMoAs drastically altered the link between individual- and population-level effects. For example, hypothetical stressors with different PMoAs that had equal effects on reproduction had effects ranging from a negligible decline in biomass to population extinction. Thus, reproduction tests alone are of little use for extrapolating toxicity to the population level, but we showed that the ecological relevance of standard tests could easily be improved if growth is measured along with reproduction.
1. Herbivores show stronger control of element homoeostasis than primary producers, which can lead to constraints in carbon and nutrient transfer efficiencies from plants to animals. Insufficient dietary phosphorus (P) availability can cause reduced body P contents along with lower growth rates of animals, leading to a positive relationship between growth and body P.
2. We examined how a second limiting food component in combination with dietary P limitation influences growth and P homoeostasis of a herbivore and how this colimitation influences the hypothesized positive correlation between body P content and growth rates. Therefore, we investigated the responses in somatic growth and P stoichiometry of Daphnia magna raised on a range of diets with different amounts of P and the sterol cholesterol.
3. Somatic growth rates of D. magna increased asymptotically with increasing P as well as with increasing cholesterol availability. The body P content increased with increasing dietary P and stabilized at high dietary P availability. The observed plasticity in D. magna's P stoichiometry became stronger with increasing cholesterol availability, i.e. with decreasing colimitation by cholesterol.
4. At P-limiting conditions, the positive correlation between body P content and growth rate, as predicted by the growth rate hypothesis (GRH) applied to the within-species level, declined with increasing cholesterol limitation and disappeared entirely when cholesterol was not supplied. Thus, even when Daphnia shows no growth response owing to strong limitation by the colimiting nutrient, the body P content may vary substantially, calling into question the unconditional use of herbivores' P content as predictor of a potential P limitation in nature.
5. The observed interaction between dietary P and cholesterol on Daphnia's growth and stoichiometry can be used as a conceptual framework of how colimiting essential nutrients affect herbivore homoeostasis, and provide further insights into the applicability of the GRH within a consumer species.
Dietary lipid quality affects temperature-mediated reaction norms of a freshwater key herbivore
(2012)
Temperature-mediated plasticity in life history traits strongly affects the capability of ectotherms to cope with changing environmental temperatures. We hypothesised that temperature-mediated reaction norms of ectotherms are constrained by the availability of essential dietary lipids, i.e. polyunsaturated fatty acids (PUFA) and sterols, as these lipids are involved in the homeoviscous adaptation of biological membranes to changing temperatures. A life history experiment was conducted in which the freshwater herbivore Daphnia magna was raised at four different temperatures (10, 15, 20, 25A degrees C) with food sources differing in their PUFA and sterol composition. Somatic growth rates increased significantly with increasing temperature, but differences among food sources were obtained only at 10A degrees C at which animals grew better on PUFA-rich diets than on PUFA-deficient diets. PUFA-rich food sources resulted in significantly higher population growth rates at 10A degrees C than PUFA-deficient food, and the optimum temperature for offspring production was clearly shifted towards colder temperatures with an increased availability of dietary PUFA. Supplementation of PUFA-deficient food with single PUFA enabled the production of viable offspring and significantly increased population growth rates at 10A degrees C, indicating that dietary PUFA are crucial for the acclimation to cold temperatures. In contrast, cumulative numbers of viable offspring increased significantly upon cholesterol supplementation at 25A degrees C and the optimum temperature for offspring production was shifted towards warmer temperatures, implying that sterol requirements increase with temperature. In conclusion, essential dietary lipids significantly affect temperature-mediated reaction norms of ectotherms and thus temperature-mediated plasticity in life history traits is subject to strong food quality constraints.