Molecular evidence for metazooplankton feeding on filamentous cyanobacteria and picocyanobacteria in the Baltic Sea
Sammanfattning: Interactions between zooplankton and cyanobacteria are complex and system-specific. They play an important role in mediating responses of phytoplankton to changes in nutrient regime and top-down manipulations. Negative consequences associated with these interactions include massive blooms of diazotrophic blue-green algae and declines in zooplankton and fish stocks. With regard to filamentous cyanobacteria, toxicity, morphology, and poor nutritional quality have commonly been implicated as mechanisms hampering efficient grazing, whereas picocyanobacteria are generally considered as inaccessible for mesozooplankton grazers due to their small size. The evidence for these assumptions are, however, contradictory, and there are studies showing that both picocyanobacteria and filamentous cyanobacteria can contribute substantially to zooplankton diets. Moreover, by supplying nitrogen to non-diazotrophic phytoplankton, these cyanobacterial blooms fuel production of edible phytoplankton and picoplankton, including picocyanobacteria. Thus, cyanobacteria could have a neutral or even positive effect on growth of mesozooplankton. As zooplankton is the main trophic link between primary producers and higher trophic levels, it is important to understand whether mesozooplankton can efficiently utilize cyanobacterial production by direct grazing. Here, I used molecular approach in the field and laboratory studies to determine (1) whether pico- and filamentous cyanobacteria are ingested by mesozooplankton grazers, (2) what species/groups are particularly efficient in grazing on picocyanobacteria, and (3) consequences of feeding on toxic filamentous cyanobacterium for copepod physiological status.In Paper I, we experimentally studied effects of direct ingestion of toxic filamentous cyanobacteria on oxidative status, reproduction, and juvenile development in the copepod Acartia bifilosa. Moreover, using short- and long-term field observations on the egg production in Acartia tonsa and growth of nauplii in the common Baltic copepods Acartia spp. and Eurytemora affinis in relation to cyanobacteria abundance, we showed overall positive effects of diazotrophic filamentous cyanobacteria on oxidative balance, viable egg production and nauplial growth. These findings suggest that cyanobacterial blooms in the Baltic Sea might contribute, both directly and indirectly, to zooplankton nutrition. The indirect effects are most likely mediated through the stimulation of picoplankton communities by filamentous cyanobacteria blooms thus enhancing nutrition of zooplankton capable of utilizing picoplankton component of the microbial food webs.In Paper II, we evaluated the extent of the direct grazing by mesozooplankton on picocyanobacteria in the field as hypothesized in Paper I. The picocyanobacteria in ambient plankton communities and zooplankton guts were quantified by molecular diet analysis. The method is based on quantitative PCR (qPCR) targeting ITS-1 sequence of the picocyanobacteria Synechococcus that allowed us to measure picocyanobacterial DNA in the guts of major Baltic mesozooplankton groups (cladocerans, rotifers and various developmental stages of copepods). Also, a feeding experiment with laboratory reared copepod Acartia tonsa fed a mixture of the picocyanobacterium Synechococcus bacillaris and the cryptophyte alga Rhodomonas salina was conducted to measure picocyanobacteria consumption in the presence of the alternative food. All field-collected and experimental animals were found to consume Synechococcus spp. In terms of Synechococcus quantity, the individual gut content was highest in the cladocerans, whereas biomass-specific gut content was highest in the rotifers and the copepod nauplii. The amount of Synechococcus DNA in the guts of the field-collected copepods was positively related to the picocyanobacteria abundance and negatively to the total phytoplankton (> 2 µm) stocks at the time of sampling. This indicates that increased availability of picocyanobacteria resulted in the increased intake of this prey and that copepods may rely more on this prey when preferred food declines. These findings suggest that if abundant, picoplankton is an important component of mesozooplankton diet, which needs to be accounted for in food web models and productivity assessments.
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