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

Selective Grazing by a Tropical Copepod (Notodiaptomus iheringi) Facilitates Microcystis Dominance

Top-down grazer control of cyanobacteria is a controversial topic due to conflicting reports of success and failure as well as a bias toward studies in temperate climates with large generalist grazers like Daphnia. In the tropical lowland lakes of Brazil, calanoid copepods of the Notodiaptomus complex dominate zooplankton and co-exist in high abundance with permanent blooms of toxic cyanobacteria, raising questions for grazer effects on bloom dynamics (i.e., top-down control vs. facilitation of cyanobacterial dominance). Accordingly, the effect of copepod grazing on the relative abundance of Microcystis co-cultured with a eukaryotic phytoplankton (Cryptomonas) was evaluated in a series of 6-day laboratory experiments. Grazer effects were tested in incubations where the growth of each phytoplankton in the presence or absence of the copepod Notodiaptomus iheringi was monitored in 1 L co-cultures, starting with a 6-fold initial dominance of Cryptomonas by biomass. Compared to the no grazer controls, N. iheringi reduced the growth of both phytoplankton, but Cryptomonas growth was reduced to negative values while Microcystis growth continued positively despite grazers. Hence, in a matter of 6 days selective grazing by N. iheringi increased the biomass of Microcystis relative to Cryptomonas by an order of magnitude compared to controls, and thus, facilitated the dominance of this cyanobacterium. To account for the potential effect of allelopathy, we performed a secondary experiment comparing the abundance and growth rate of Microcystis and Cryptomonas in single and mixed co-cultures in the absence of grazers. The growth rate of Microcystis was unaffected by the presence or relative abundance of Cryptomonas, and vice versa, indicating no allelopathic effects. Our results suggest that selectively grazing zooplankton may facilitate cyanobacteria blooms by grazing on their eukaryotic phytoplankton competitors in nature. Given that selective grazers predominate zooplankton biomass in warmer waters, grazer facilitation of blooms may be a common but poorly understood regulator of plankton dynamics in a warmer and more eutrophic world

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