Pablo Urrutia-Cordero

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.

Linking cascading effects of fish predation and zooplankton grazing to reduced cyanobacterial biomass and toxin levels following biomanipulation.

Eutrophication has been one of the largest environmental problems in aquatic ecosystems during the past decades, leading to dense, and often toxic, cyanobacterial blooms. In a way to counteract these problems many lakes have been subject to restoration through biomanipulation. Here we combine 13 years of monitoring data with experimental assessment of grazing efficiency of a naturally occurring zooplankton community and a, from a human perspective, desired community of large Daphnia to assess the effects of an altered trophic cascade associated with biomanipulation. Lake monitoring data show that the relative proportion of Daphnia spp. grazers in June has increased following years of biomanipulation and that this increase coincides with a drop in cyanobacterial biomass and lowered microcystin concentrations compared to before the biomanipulation. In June, the proportion of Daphnia spp. (on a biomass basis) went from around 3% in 2005 (the first year of biomanipulation) up to around 58% in 2012. During months when the proportion of Daphnia spp. remained unchanged (July and August) no effect on lower trophic levels was observed. Our field grazing experiment revealed that Daphnia were more efficient in controlling the standing biomass of cyanobacteria, as grazing by the natural zooplankton community never even compensated for the algal growth during the experiment and sometimes even promoted cyanobacterial growth. Furthermore, although the total cyanobacterial toxin levels remained unaffected by both grazer communities in the experimental study, the Daphnia dominated community promoted the transfer of toxins to the extracellular, dissolved phase, likely through feeding on cyanobacteria. Our results show that biomanipulation by fish removal is a useful tool for lake management, leading to a top-down mediated trophic cascade, through alterations in the grazer community, to reduced cyanobacterial biomass and lowered cyanobacterial toxin levels. This improved water quality enhances both the ecological and societal value of lakes as units for ecosystem services.

Local food web management increases resilience and buffers against global change effects on freshwaters

A major challenge for ecological research is to identify ways to improve resilience to climate-induced changes in order to secure the ecosystem functions of natural systems, as well as ecosystem services for human welfare. With respect to aquatic ecosystems, interactions between climate warming and the elevated runoff of humic substances (brownification) may strongly affect ecosystem functions and services. However, we hitherto lack the adaptive management tools needed to counteract such global-scale effects on freshwater ecosystems. Here we show, both experimentally and using monitoring data, that predicted climatic warming and brownification will reduce freshwater quality by exacerbating cyanobacterial growth and toxin levels. Furthermore, in a model based on long-term data from a natural system, we demonstrate that food web management has the potential to increase the resilience of freshwater systems against the growth of harmful cyanobacteria, and thereby that local efforts offer an opportunity to secure our water resources against some of the negative impacts of climate warming and brownification. This allows for novel policy action at a local scale to counteract effects of global-scale environmental change, thereby providing a buffer period and a safer operating space until climate mitigation strategies are effectively established.

Controlling Harmful Cyanobacteria: Taxa-Specific Responses of Cyanobacteria to Grazing by Large-Bodied Daphnia in a Biomanipulation Scenario.

Lake restoration practices based on reducing fish predation and promoting the dominance of large-bodied Daphnia grazers (i.e., biomanipulation) have been the focus of much debate due to inconsistent success in suppressing harmful cyanobacterial blooms. While most studies have explored effects of large-bodied Daphnia on cyanobacterial growth at the community level and/or on few dominant species, predictions of such restoration practices demand further understanding on taxa-specific responses in diverse cyanobacterial communities. In order to address these questions, we conducted three grazing experiments during summer in a eutrophic lake where the natural phytoplankton community was exposed to an increasing gradient in biomass of the large-bodied Daphnia magna. This allowed evaluating taxa-specific responses of cyanobacteria to Daphnia grazing throughout the growing season in a desired biomanipulation scenario with limited fish predation. Total cyanobacterial and phytoplankton biomasses responded negatively to Daphnia grazing both in early and late summer, regardless of different cyanobacterial densities. Large-bodied Daphnia were capable of suppressing the abundance of Aphanizomenon, Dolichospermum, Microcystis and Planktothrix bloom-forming cyanobacteria. However, the growth of the filamentous Dolichospermum crassum was positively affected by grazing during a period when this cyanobacterium dominated the community. The eutrophic lake was subjected to biomanipulation since 2005 and nineteen years of lake monitoring data (1996–2014) revealed that reducing fish predation increased the mean abundance (50%) and body-size (20%) of Daphnia, as well as suppressed the total amount of nutrients and the growth of the dominant cyanobacterial taxa, Microcystis and Planktothrix. Altogether our results suggest that lake restoration practices solely based on grazer control by large-bodied Daphnia can be effective, but may not be sufficient to control the overgrowth of all cyanobacterial diversity. Although controlling harmful cyanobacterial blooms should preferably include other measures, such as nutrient reductions, our experimental assessment of taxa-specific cyanobacterial responses to large-bodied Daphnia and long-term monitoring data highlights the potential of such biomanipulations to enhance the ecological and societal value of eutrophic water bodies.