SUMMARY1. We review and update recent observations of cyanobacteria-zooplankton interactions, identify theoretical and methodological limitations and evaluate approaches necessary for understanding the effects of increasing cyanobacterial blooms on plankton dynamics. 2. The emphasis on oversimplified studies using large-bodied Daphnia species, not previously exposed to cyanobacteria, has limited our understanding of how the plankton responds to proliferating blooms. This overlooks the great diversity in zooplankton traits, and the adaptability of planktonic grazers, that enables them to deal with toxic prey. 3. Under increasing temperature and nutrient loading, the zooplankton will be subjected to increasingly intense selection pressure to tolerate cyanobacteria. Short zooplankton generation times suggest that increased blooms may select for the rapid evolution of behavioural and physiological traits that improve tolerance. 4. As eutrophication intensifies, should we expect physiologically tolerant zooplankton that may be able to control blooms, or be concerned with the effects of selective grazers in stabilising blooms? 5. We conclude that the increasing frequency, duration and intensity of blooms will select for better adapted zooplankton that coexist with, rather than control, cyanobacteria. Future evaluations of cyanobacteria-zooplankton interactions should consider that increasing exposure to blooms induces phenotypic and genotypic traits improving zooplankton tolerance. Equally important will be studies of the ecophysiology of zooplankton species that coexist with prolonged blooms, rather than those of a few large-bodied generalist cladocerans. 6. Since cyanobacteria produce more than one toxic or inhibitory metabolite, the unsystematic designation of toxicity based on single well-identified compounds (e.g. microcystin) should be revised. 7. Overall, the coevolutionary interaction between cyanobacterial defences and zooplankton grazer responses emerges as a critical but understudied regulator of bloom dynamics.
Toxicity and morphology may function as defense mechanisms of bloom-forming cyanobacteria against zooplankton grazing. Yet, the relative importance of each of these factors and their plasticity remains poorly known. We tested the effects of chemical and morphological traits of the bloom-forming cyanobacterium Cylindrospermopsis raciborskii on the feeding response of the selective feeder Eudiaptomus gracilis (Calanoida, Copepoda), using a saxitoxin-producing strain (STX+) and a non-saxitoxin (STX−)-producing strain as food. From these two chemotypes, we established cultures of three different morphotypes that differed in filament length (short, medium, and long) by incubating the strains at 17, 25, and 32 °C. We hypothesized that the inhibitory effects of saxitoxins determine the avoidance of C. raciborskii, and that morphology would only become relevant in the absence of saxitoxins. Temperature affected two traits: higher temperature resulted in significantly shorter filaments in both strains and led to much higher toxin contents in the STX+ strain (1.7 μg eq STX L−1 at 17 °C, 7.9 μg eq STX L−1 at 25 °C, and 25.1 μg eq STX L−1 at 32 °C). Copepods strongly reduced the ingestion of the STX+ strain in comparison with STX− cultures, regardless of filament length. Conversely, consumption of shorter filaments was significantly higher in the STX− strain. The great plasticity of morphological and chemical traits of C. raciborskii and their resultant contrasting effects on the feeding behavior of zooplankton might explain the success of this cyanobacterium in a variety of aquatic environments.Electronic supplementary materialThe online version of this article (doi:10.1007/s00248-016-0734-8) contains supplementary material, which is available to authorized users.
We tested the hypothesis that calanoid copepods would adapt to extended periods of Microcystis exposure by increasing selective feeding on alternative food. Copepod (Eudiaptomus gracilis) clearance rates were compared before and after a 5-d acclimation to Microcystis aeruginosa using paired food mixtures containing a microcystinproducing (MC+) or -lacking (MC2) strain and the green alga Chlamydomonas reinhardtii. Acclimation reduced the ingestion of Microcystis, increased ingestion of Chlamydomonas, and subsequently increased feeding selectivity. The effect of acclimation was more pronounced for food mixtures with MC+ Microcystis, suggesting that E. gracilis uses a strain-specific cue related to microcystin or microcystin itself to avoid harmful food. The results indicate that exposure to sublethal abundances of Microcystis may increase copepod tolerance to blooms, given sufficient alternative food. Zooplankton grazing behavior should, therefore, be viewed as flexible and adaptive to extended periods of cyanobacteria blooms.
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.
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.
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