Consumers feeding at the aquatic–terrestrial ecosystem interface may obtain a mixture of aquatic and terrestrial diet resources that vary in nutritional composition. However, in lake riparian ...spiders, the relative significance of aquatic versus terrestrial diet sources remains to be explored. We investigated the trophic transfer of lipids and polyunsaturated fatty acids (PUFA) from emergent aquatic and terrestrial insects to spiders at varying distances from the shoreline of a subalpine lake in Austria, using differences in fatty acid profiles and compound‐specific stable carbon (δ13C) and hydrogen (δ2H) isotopes. The omega‐3 PUFA content of emergent aquatic insects was higher than that of terrestrial insects. Emergent aquatic insects contained on average 6.6 times more eicosapentaenoic acid (EPA) and 1.2 times more α‐linolenic acid (ALA) than terrestrial insects, whereas terrestrial insects contained on average 2.6 times more linoleic acid (LIN) than emergent aquatic insects. Spiders sampled directly on the lake and in upland habitats had similar EPA contents, but this EPA was derived from different diet sources, depending on the habitat. The δ13CEPA and δ2HEPA values of ‘lake spiders' revealed an aquatic diet pathway (i.e. EPA of aquatic origin). In contrast, EPA of spiders collected in terrestrial habitats was depleted in both 13C and 2H compared to any potential food sources, and their ALA isotopic values, suggesting that EPA was partly bioconverted from its dietary precursor ALA (i.e. internal pathway). The δ2H values of fatty acids clearly indicated that diet sources differed depending on the spider's habitat, which was less evident from the δ13C values of the fatty acids. Our data highlight that spiders can use two distinct pathways (trophic versus metabolic) to satisfy their physiological EPA demand, depending on habitat use and dietary availability.
Inducible morphological defences are crucial for understanding predator–prey interactions. Such defences have been mostly studied in a single‐predator context, ignoring the fact that prey organisms ...are often exposed to multiple predators. In deep peri‐Alpine European lakes, the keystone grazer Daphnia coexists with two cladoceran predators, Bythotrephes longimanus and Leptodora kindtii. Up to now, life history and morphological responses of Daphnia to these two predators have not been analysed systematically.
We studied the responses of two life history (age at first reproduction, and offspring production) and five morphological traits (body size, body width, head size, spina size, and eye diameter) of eight Daphnia galeata clones to the presence of Bythotrephes and Leptodora in a common garden experiment. We compared each response trait between treatments using linear mixed models, and investigated the covariation between defence traits and demographic costs (neonate production) for the two predators.
Our results show that the responses of Daphnia are predator‐ and trait‐specific. Daphnia developed a typical helmet and a larger eye only in the presence of Bythotrephes, not in the presence of Leptodora. In contrast, both predators induced larger body sizes and longer spines. Age at first reproduction was latest and demographic costs were highest in the Bythotrephes treatment, suggesting that the development of a helmet exceeds the costs of spina elongation. The responses of Daphnia clones revealed a defence‐cost trade‐off for helmet formation in the Bythotrephes, and for spina elongation in the Leptodora treatment. Hence, despite Bythotrephes and Leptodora being closely related co‐occurring predators, Daphnia responds with a unique combination of trait changes and defence‐cost trade‐offs to the two predators.
The presence of predator‐specific clonal defence‐cost trade‐offs suggests that the presence of these invertebrate predators can drive different evolutionary processes in natural zooplankton communities. Disentangling the evolutionary ecology of phenotypic responses of prey species to co‐occurring predators will require multi‐trait, multi‐clone studies of induced antipredator defences.
Zooplankton displays different inducible defenses against invertebrate and vertebrate predators. The response pattern to gape‐limited invertebrate predators involves increased somatic growth and ...offspring body size but delayed maturity and reduced offspring numbers. In contrast to this general pattern, the freshwater model organism Daphnia magna has been reported to exhibit a different response when encountering the gape‐limited tadpole shrimp Triops cancriformis. Under laboratory conditions, D. magna showed increased somatic growth, earlier maturation, and an increase in both offspring number and size. We propose here that the discrepancy between the previously observed and the theory‐based response patterns against invertebrate predators is due to differences in food availability in the applied laboratory settings and assessed whether the defensive response of D. magna against T. cancriformis is modulated differently by food quantity and quality. We found a strong impact of food quantity and quality on the defense response of D. magna to T. cancriformis kairomones. The prey seem to be able to overcome trade‐offs between morphological defense traits and reproductive traits, but distinctly between high food quantity and high food quality. Thereby, reproductive traits were preferred over morphological defenses. Furthermore, the removal of particles from the T. cancriformis‐conditioned water caused a defense pattern in D. magna that was consistent with the general response pattern known from other invertebrate predators, thus explaining the described discrepancy to previous studies with T. cancriformis. Our study highlights the importance of assessing food‐related effects on predator–prey interactions to understand trophic relationships and food web processes.
Essential biomolecules can critically influence the performance of consumers. A deficiency in dietary sterols has been shown to constrain the food quality of prokaryotic food sources for aquatic ...consumers. Here, we assessed the importance of dietary cholesterol for life history traits (survival, growth and egg production) of the freshwater herbivore Daphnia magna in supplementation experiments with various sterol‐containing eukaryotic phytoplankton diets (dinoflagellates, diatoms, and golden algae). We combined cholesterol supplementation via liposomes with 13C‐labelling of the phytoplankton diets and traced the origin of cholesterol in Daphnia using compound‐specific stable isotope analysis. All phytoplankton strains used here were rich in polyunsaturated fatty acids (PUFA) but differed in their phytosterol composition. We show that growth and reproduction of D. magna can be limited by sterols even when feeding on sterol‐containing eukaryotic phytoplankton diets. The impact of cholesterol supplementation on growth and reproduction of D. magna differed among phytoplankton diets (strains). The positive effect of cholesterol supplementation was most pronounced on diatom diets. Estimation of source proportions using stable isotopes revealed that D. magna preferentially assimilated the supplemented cholesterol rather than synthesizing it from dietary phytosterols. Our experiments suggest that the different responses to cholesterol supplementation on the various phytoplankton diets were unrelated to the suitability of dietary phytosterols to serve as cholesterol precursors but were caused by other biochemical or morphological food quality constraints. The combination of methods applied here could be very useful for uncovering nutritional constraints and thus for assessing the importance of essential biomolecules for the performance of herbivorous consumers.
Ecology Letters (2011)
There is growing consensus that the growth of herbivorous consumers is frequently limited by more than one nutrient simultaneously. This understanding, however, is based ...primarily on theoretical considerations and the applicability of existing concepts of co‐limitation has rarely been tested experimentally. Here, we assessed the suitability of two contrasting concepts of resource limitation, i.e. Liebig’s minimum rule and the multiple limitation hypothesis, to describe nutrient‐dependent growth responses of a freshwater herbivore (Daphnia magna) in a system with two potentially limiting nutrients (cholesterol and eicosapentaenoic acid). The results indicated that these essential nutrients interact, and do not strictly follow Liebig’s minimum rule, which consistently overestimates growth at co‐limiting conditions and thus is not applicable to describe multiple nutrient limitation of herbivorous consumers. We infer that the outcome of resource‐based modelling approaches assessing herbivore population dynamics strongly depends on the applied concept of co‐limitation.
Organisms at the base of aquatic food webs synthesize essential nutrients, such as omega‐3 polyunsaturated fatty acids (n‐3 PUFA), which are transferred to consumers at higher trophic levels. Many ...consumers, requiring n‐3 long‐chain (LC) PUFA, such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), have limited ability to biosynthesize them from the essential dietary precursor α‐linolenic acid (ALA) and thus rely on dietary provision of LC‐PUFA.
We investigated LC‐PUFA metabolism in freshwater zooplankton using stable hydrogen isotopes (δ2H) of fatty acids as tracers. We conducted feeding experiments with the freshwater keystone grazer Daphnia to quantify changes in the δ2H value of body FA in response to the FA composition of their food and the δ2H value of the ambient water.
The isotopic composition of LC‐PUFA changed in Daphnia, depending on the integration of 2H from ambient water during de novo synthesis or bioconversion from dietary precursors, allowing us to distinguish dietary from bioconverted EPA in body tissue. We tested the applicability of these laboratory findings in a field setting by analysing δ2H values of PUFA in primary producers and consumers in eutrophic ponds to track EPA sources of zooplankton.
Multilinear regression models that included conversion of ALA to EPA correlated better with zooplankton δ2HEPA than seston δ2HEPA at low dietary EPA supply.
This study provides evidence that zooplankton can compensate for low dietary EPA supply by activating LC‐PUFA biosynthesis and shows that herbivorous zooplankton play a crucial role in upgrading FA for higher trophic levels during low dietary EPA supply.
A free Plain Language Summary can be found within the Supporting Information of this article.
A free Plain Language Summary can be found within the Supporting Information of this article.
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.
Summary
Chytrids are ubiquitous fungal parasites in aquatic ecosystems, infecting representatives of all major phytoplankton groups. They repack carbon from inedible phytoplankton hosts into easily ...ingested chytrid propagules (zoospores), rendering this carbon accessible to zooplankton. Grazing on zoospores may circumvent bottlenecks in carbon transfer imposed by the dominance of inedible or poorly nutritious phytoplankton (mycoloop). We explored qualitative aspects of the mycoloop by analysing lipid profiles (fatty acids, sterols) of two chytrids infecting two major bloom‐forming phytoplankton taxa of contrasting nutritional value: the diatom Asterionella formosa and the filamentous cyanobacterium Planktothrix agardhii. The polyunsaturated fatty acid composition of chytrids largely reflected that of their hosts, highlighting their role as conveyors of otherwise inaccessible essential lipids to higher trophic levels. We also showed that chytrids are capable of synthesizing sterols, thus providing a source of these essential nutrients for grazers even when sterols are absent in their phytoplankton hosts. Our findings reveal novel qualitative facets of the mycoloop, showing that parasitic chytrids, in addition to making carbon and essential lipids available from inedible sources, also upgrade their host's biochemical composition by producing sterols de novo, thereby enhancing carbon and energy fluxes in aquatic food webs.
Blooms of the red, filamentous cyanobacterium Planktothrix rubescens occur frequently in pre-alpine lakes in Europe, often with concomitant toxic microcystin (MC) production. Trophic transfer of MCs ...has been observed in bivalves, fish, and zooplankton species, while uptake of MCs into Diptera species could facilitate distribution of MCs into terrestrial food webs and habitats. In this study, we characterized a Planktothrix bloom in summer 2019 in Lake Mindelsee and tracked possible trophic transfer and/or bioaccumulation of MCs via analysis of phytoplankton, zooplankton (Daphnia) and emergent aquatic insects (Chaoborus, Chironomidae and Trichoptera). Using 16 S rRNA gene amplicon sequencing, we found that five sequence variants of Planktothrix spp. were responsible for bloom formation in September and October of 2019, and these MC-producing variants, provisionally identified as P. isothrix and/or P. serta, occurred exclusively in Lake Mindelsee (Germany), while other variants were also detected in nearby Lake Constance. The remaining cyanobacterial community was dominated by Cyanobiaceae species with high species overlap with Lake Constance, suggesting a well-established exchange of cyanobacteria species between the adjacent lakes. With targeted LC–HRMS/MS we identified two MC-congeners, MC-LR and Asp3MC-RR with maximum concentrations of 45 ng Asp3MC-RR/L in lake water in September. Both MC congeners displayed different predominance patterns, suggesting that two different MC-producing species occurred in a time-dependent manner, whereby Asp3MC-RR was clearly associated with the Planktothrix spp. bloom. We demonstrate an exclusive transfer of MC-LR, but not Asp3MC-RR, from phytoplankton into zooplankton reaching a 10-fold bioconcentration, yet complete absence of these MC congeners or their conjugates in aquatic insects. The latter demonstrated a limited trophic transfer of MCs from zooplankton to zooplanktivorous insect larvae (e.g., Chaoborus), or direct transfer into other aquatic insects (e.g. Chironomidae and Trichoptera), whether due to avoidance or limited uptake and/or rapid excretion of MCs by higher trophic emergent aquatic insects.
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•A Planktothrix sp. bloom specific to Lake Mindelsee produced the toxin Asp3MC-RR.•MC-LR-transfer from Microcystis sp. to zooplankton resulted in MC-biomagnification.•MC or MC metabolite-trophic transfer to emergent aquatic insects was not detected.•No toxic Planktothrix sp. blooms were reported in the adjacent Lake Constance.•Synechococcus phylotypes of Lake Mindelsee are potentially exchanged between lakes.
Diel vertical migration (DVM) is a common predator avoidance strategy of zooplankton. Migration to deeper water layers during the day to escape visually hunting predators is most likely to require ...physiological adaptations to periodically changing temperatures. Polyunsaturated fatty acids (PUFA) play crucial roles in membrane temperature acclimation. Exposure to cold temperatures typically results in an increase in the relative abundance of PUFA in cell membranes and PUFA requirements of Daphnia increase with decreasing temperatures.
To assess the role of dietary PUFA in coping with temperature fluctuations experienced during DVM, we reared Daphnia magna at either constantly warm or fluctuating temperatures, simulating DVM both with and without dietary PUFA supplementation.
We show that the well‐known positive effect of dietary eicosapentaenoic acid supplementation on offspring production and population growth rates of D. magna is more pronounced at alternating temperatures than at constantly warm temperatures. Exposure to alternating temperatures caused modification in body PUFA concentrations and, consequently, increased lipid peroxidation. However, detrimental effects of lipid peroxidation were not evident.
Our data demonstrate that the capacity to cope with the distinct temperature fluctuations experienced during DVM increases with dietary eicosapentaenoic acid supplementation, suggesting that an adequate dietary PUFA supply is crucial especially for migrating Daphnia populations. A dietary deficiency in long‐chain PUFA may thus severely constrain predator evasion, potentially resulting in increased mortality and cascading effects on lower trophic levels.
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