Environmental variability in aquatic ecosystems: Avenues for future multifactorial experiments

The relevance of considering environmental variability for understanding and predicting biological responses to environmental changes has resulted in a recent surge in variability-focused ecological research. However, integration of findings that emerge across studies and identification of remaining knowledge gaps in aquatic ecosystems remain critical. Here, we address these aspects by: (1) summarizing relevant terms of variability research including the components (characteristics) of variability and key interactions when considering multiple environmental factors; (2) identifying conceptual frameworks for understanding the consequences of environmental variability in single and multifactorial scenarios; (3) highlighting challenges for bridging theoretical and experimental studies involving transitioning from simple to more complex scenarios; (4) proposing improved approaches to overcome current mismatches between theoretical predictions and experimental observations; and (5) providing a guide for designing integrated experiments across multiple scales, degrees of control, and complexity in light of their specific strengths and limitations

Beyond Daphnia: a plea for a more inclusive and unifying approach to freshwater zooplankton ecology

Zooplankton plays a pivotal role in lentic water bodies, linking planktonic primary producers to higher trophic levels and being a cornerstone of the planktonic food web of ponds and lakes. Because of its ease of culture, large size, rich ecology, abundance in northern temperate lakes where limnology is rooted, and the ability to work with clones, Daphnia has, in the last centuries grown to become a key model system in ecology, evolution, and ecotoxicology. Consequently, a vast majority of freshwater zooplankton ecology focuses on the role of Daphnia. While generating essential insights, this has also deviated attention from the broad ecological impact of other zooplankton. Here, we emphasize how other zooplankton taxa have an important impact in nature - often in qualitatively different ways than Daphnia. We illustrate this point by focusing on two key zooplankton functions (herbivory and stoichiometry) and suggest research to capitalize on the success story of mechanistic ecological, eco-evolutionary, and genomic Daphnia work to develop a richer set of model organisms. We currently have the tools to do so and integrating mechanistic insights in multispecies settings would foster a better understanding of the rich diversity and ecology of freshwater zooplankton

Zooplankton grazing selectivity regulates herbivory and dominance of toxic phytoplankton over multiple prey generations

How grazer selectivity regulates the primary producer community is a core topic in ecology. Yet, the role of zooplankton grazing selection on phytoplankton dynamics is poorly understood. Few studies have compared the effect of grazers with contrasting selectivity on mixed phytoplankton prey, and none over multiple phytoplankton generations. We tested the hypothesis that a selectively grazing copepod (Eudiaptomus gracilis) would facilitate the dominance of a toxic cyanobacterium (Microcystis aeruginosa) by grazing on a competing eukaryotic microalga (Cryptomonas pyrenoidifera), while a generalist cladoceran (Daphnia magna) would have no effect on the dominance of cyanobacteria in 4-d laboratory cocultures. Experiments started with a ninefold initial dominance of Cryptomonas over Microcystis by biomass. Each grazer type was added to cocultured phytoplankton and the abundance of phytoplankton was compared to no-grazer controls. As predicted, Daphnia had no effect on the relative abundance of its prey and the copepod facilitated Microcystis dominance, although the strength of facilitation slightly declined with time. As the copepod reduced mostly the biomass of the edible algae, it pushed the system toward the dominance of toxic prey, which likely reduced the efficiency of selective grazing on the last day. Hence, while the selective grazer promoted cyanobacterial dominance, the effect may be weaker than predicted from extrapolating grazing rates obtained from short-term (i.e., hourly) assays. Overall, predicting the role of zooplankton selectivity on phytoplankton dynamics—especially harmful algal blooms—would benefit from accounting for fluctuations in grazer effects due to shifting abundance and growth of each prey over time.</p

Effect of the toxin (microcystin) content of Microcystis on copepod grazing

Although phytoplankton chemical defense may regulate plankton dynamics, demonstrating an ecologically relevant anti-grazer cue is challenging. Presented here is a novel approach to evaluate the quantitative effect of microcystin (MC), the most studied group of cyanobacterial metabolites, on grazing by the common copepod Eudiaptomus gracilis. A temperature-induced gradient in the intracellular MC concentration of three different Microcystis strains enabled the comparison of grazing pressure on cells of the same cyanobacterial strain producing different amounts of MC, in a diet with alternative food (Chlamydomonas). In all treatments, grazing pressure on Microcystis was inversely related to its MC-LR content, while selection for alternative prey was positively related to the MC-LR content of Microcystis. Moreover, grazing on Chlamydomonas also declined with increasing Microcystis MC-LR content, suggesting toxicity related inhibition of E. gracilis. The negative relation between cellular MC-LR concentration and feeding responses supported the anti-grazer hypothesis. Not all MC variants responded to temperature, and some were therefore not associated to grazing responses. Using an induced gradient in the concentration of a suspected phytoplankton defense metabolite to evaluate its quantitative relationship with grazing pressure offers an improved inference on the ecological roles of toxins. Results suggest that either MC-LR or a correlating trait may be inversely linked to the grazer pressure on Microcystis

Copepod Prey Selection and Grazing Efficiency Mediated by Chemical and Morphological Defensive Traits of Cyanobacteria

Phytoplankton anti-grazer traits control zooplankton grazing and are associated with harmful blooms. Yet, how morphological versus chemical phytoplankton defenses regulate zooplankton grazing is poorly understood. We compared zooplankton grazing and prey selection by contrasting morphological (filament length: short vs. long) and chemical (saxitoxin: STX- vs. STX+) traits of a bloom-forming cyanobacterium (Raphidiopsis) offered at different concentrations in mixed diets with an edible phytoplankton to a copepod grazer. The copepod selectively grazed on the edible prey (avoidance of cyanobacteria) even when the cyanobacterium was dominant. Avoidance of the cyanobacterium was weakest for the "short STX-" filaments and strongest for the other three strains. Hence, filament size had an effect on cyanobacterial avoidance only in the STX- treatments, while toxin production significantly increased cyanobacterial avoidance regardless of filament size. Moreover, cyanobacterial dominance reduced grazing on the edible prey by almost 50%. Results emphasize that the dominance of filamentous cyanobacteria such as Raphidiopsis can interfere with copepod grazing in a trait specific manner. For cyanobacteria, toxin production may be more effective than filament size as an anti-grazer defense against selectively grazing zooplankton such as copepods. Our results highlight how multiple phytoplankton defensive traits interact to regulate the producer-consumer link in plankton ecosystems

Cyanobacteria dominance drives zooplankton functional dispersion

Accelerated eutrophication reduces water quality and shifts plankton communities. However, its effects on the aquatic food web and ecosystem functions remain poorly understood. Within this context, functional ecology can provide valuable links relating community traits to ecosystem functioning. In this study, we assessed the effects of eutrophication and cyanobacteria blooms on zooplankton functional diversity in a tropical hypereutrophic lake. Phytoplankton and zooplankton communities and limnological characteristics of a tropical Brazilian Lake (Southeast, Brazil) were monitored monthly from April 2013 to October 2014. Lake eutrophication indicators were total phosphorus, total chlorophyll-a, and chlorophyll-a per group (blue, green, and brown). The variation of major phytoplankton taxonomic group biomass was calculated and used as a proxy for changes in phytoplankton composition. Zooplankton functional diversity was assessed through functional dispersion and the community-weighted mean trait value. Regressions were performed between the lake eutrophication indicators, the phytoplankton biomass variation, and zooplankton functional dispersion. Our results suggest that eutrophication and cyanobacterial dominance change the composition of zooplankton traits and reduce functional dispersion, leading to zooplankton niche overlap. These findings are important because they provide a meaningful view of phytoplankton-zooplankton trophic interactions and contribute to an improved understanding their functional effects on aquatic ecosystems.</p

The interaction between cyanobacteria and zooplankton in a more eutrophic world

As blooms of cyanobacteria expand and intensify in freshwater systems globally, there is increasing interest in their ecological effects. In addition to being public health hazards, cyanobacteria have long been considered a poor quality food for key zooplankton grazers that link phytoplankton to higher trophic levels. While past laboratory studies have found negative effects of nutritional constraints and defensive traits (i.e., toxicity and colonial or filamentous morphology) on the fitness of large generalist grazers (i.e., Daphnia), cyanobacterial blooms often co-exist with high biomass of small-bodied zooplankton in nature. Indeed, recent studies highlight the remarkable diversity and flexibility in zooplankton responses to cyanobacterial prey. Reviewed here are results from a wide range of laboratory and field experiments examining the interaction of cyanobacteria and a diverse zooplankton taxa including cladocerans, copepods, and heterotrophic protists from temperate to tropical freshwater systems. This synthesis shows that longer exposure to cyanobacteria can shift zooplankton communities toward better-adapted species, select for more tolerant genotypes within a species, and induce traits within the lifetime of individual zooplankton. In turn, the function of bloom-dominated plankton ecosystems, the coupling between primary producers and grazers, the stability of blooms, and the potential to use top down biomanipulation for controlling cyanobacteria depend largely on the species, abundance, and traits of interacting cyanobacteria and zooplankton. Understanding the drivers and consequences of zooplankton traits, such as physiological detoxification and selective vs. generalist grazing behavior, are therefore of major importance for future studies. Ultimately, co-evolutionary dynamics between cyanobacteria and their grazers may emerge as a critical regulator of blooms

The importance of allochthonous organic matter quality when investigating pulse disturbance events in freshwater lakes: a mesocosm experiment

Extreme precipitation is occurring with greater frequency and intensity as a result of climate change. Such events boost the transport of allochthonous organic matter (allo-OM) to freshwater ecosystems, yet little is known about the impacts on dissolved organic matter (DOM) quality and seston elemental stoichiometry, especially for lakes in warm climates. A mesocosm experiment located in a Turkish freshwater lake was designed to simulate a pulse event leading to increased inputs of allo-OM by examining the individual effects of increasing water colour (HuminFeed (R), HF), the direct effects of the extra energetic inputs (alder tree leaf leachate, L), and the interactions of the single treatment effects (combination of both sources, HFL), along with a comparison with unmanipulated controls. Changes in the DOM quality and nutrient stoichiometry of the allo-OM treatment additions was examined over the course of the experiments. Results indicated that there was an increase of high recalcitrant DOM components in the HF treatment, in contrast to an increase in less aromatic microbially derived molecules for the L treatment. Unexpectedly, seston C:P ratios remained below a severe P-limiting threshold for plankton growth and showed the same temporal pattern in all mesocosms. In contrast, seston N:P ratios differed significantly between treatments, with the L treatment reducing P-limiting conditions, whilst the HF treatment increased them. The effects of the combined HFL treatment indicated an additive type of interaction and chlorophyll-a was highest in the HFL treatment. Our results demonstrate that accounting for the optical and stoichiometric properties of experimental allo-OM treatments is crucial to improve the capacity to explain extrapolated conclusions regarding the effects of climate driven flooding on freshwater ecosystems in response to global climate change