Microbial food webs in hypertrophic fishponds: omnivorous ciliate taxa are major protistan bacterivores
Small bacterivorous protists play a fundamental role in aquatic food webs and their taxonomic classification and ecological traits currently belong to core topics in aquatic microbial ecology. Despite the importance of shallow lakes worldwide, knowledge of microbial components, the base of their food webs, remains scarce. To close this gap, we investigated planktonic microbial food webs, in particular protistan bacterivory (for both ciliates and heterotrophic nanoflagellates – HNF), in ten shallow hypertrophic fishponds in South Bohemia (Czech Republic).
We used fluorescently labeled bacteria (FLB) as bacterivory tracers to estimate how abundant protistan populations in fishponds contribute to total bacterial mortality. Fluorescence microscopy, innovative image processing tools, and quantitative protargol staining were combined to detect major bacterivorous and omnivorous ciliate taxa (see examples in Figures 1 and 2). We quantified bacterial production, bacterivory by individual ciliate species, total ciliates, and total protistan bacterivory in all fishponds. On average, ciliate bacterivory was even more important than that of HNF, accounting for 56% and 44% of total protistan grazing, respectively. Thus, the original view of a minor role of ciliate bacterivory, proposed in previous reviews of this topic for pelagic systems, may require some revision.
Figure 1 (left). Examples of major bacterivorous ciliate morphospecies in ponds: Stichotrichia and Oligotrichia. a–d, Halteria/Pelagohalteria, a zoochlorellae-bearing individual shown in d; e–h, two morphotypes of the Rimostrombidium complex with remarkable uptake of small algae along with FLB. Left side (a, c, e, g) – a protargol-stained cell, right side (b, d, f, h) – examples of the same species in fluorescence microscopy based on composite overlay of 10–20 images taken in 3 wavelengths (blue: DAPI-excitation visualizing mainly nuclei of ciliates, yellow: DTAF-excitation visualizing fluorescently labeled bacteria (FLB) uptake, red: chlorophyll excitation visualizing natural phytoplankton cells ingested in food vacuoles). The common presence of FLB and red phytoplankton cells in food vacuoles documents the ciliate omnivory. The scale bar shows length of 10 μm.
Figure 2 (right). Examples of major bacterivorous ciliate morphospecies in ponds: Peritrichia. a–b, Pelagovorticella natans; c–f, a colony of Epistylis procumbens. For more details see the Figure 1 caption.
Moreover, general ecological theories assume that specialized bacterivorous ciliates should be a prominent group of ciliates in hypertrophic aquatic environments, extremely rich in bacterial numbers and biomass. However, we found that primarily bacterivorous Peritrichia (genera Vorticella, Epistylis) and Scuticociliata (Cyclidium spp.) contributed only moderately (mean 26%) to total ciliate bacterivory. Unexpectedly, but highly abundant omnivorous Halteria/Pelagohalteria (Stichotrichia) and, to a lesser extent, also omnivorous Rimostrombidium spp. (Oligotrichia), contributed significantly more (mean 71%) to total ciliate bacterivory than typical bacterivorous taxa. This suggests that unselective omnivorous grazers which feed on a broader size spectrum from bacteria to small algae may have a considerable competitive advantage in hypertrophic environments rich in small particles. Moreover, a meta-analysis of available literature data supports our hypothesis that the role of ciliate bacterivory increases significantly, relative to HNF bacterivory, along a trophic gradient towards hypertrophic habitats (see Figure 3).
Figure 3. The meta-analysis of the relationship between chlorophyll a concentrations (as a proxy of trophic status of lakes) and proportion of bacterial standing stock grazed daily by ciliates; shown as log-log linear regression (a dashed line). The studied systems were analyzed together with the available literature data from various lakes along the trophic gradient from oligotrophy to extreme hypertrophy (n = 46). Note that all hypetrophic systems are plotted as red symbols.
Šimek K., Grujčić V., Nedoma J., Jezberová J., Šorf M., Matoušů A., Pechar L., Posch T., Bruni E. P., Vrba J. 2019: Microbial food webs in hypertrophic fishponds: omnivorous ciliate taxa are major protistan bacterivores. Limnology and Oceanography 64: 2295–2309. doi: 10.1002/lno.11260.
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