**2.2 Bacterivores**

Ciliates and flagellates are the most dominant bacterivores among the phagotrophic protists in most aquatic systems [16, 34], consuming between 25–100% of the daily production of marine phytoplankton together with large quantities of bacterial biomass [18]. Bacterivores and algivorous protists are the core consumers of microbial biomass in aquatic food webs [16, 17] regulating these groups in two apparently contradictory ways: by feeding on the abundant food source, they keep in check their further expansion, that in turn gives other less preyed species the opportunity to become more numerous, and at the same time, the release of cellular wastes (from protists) enhance the reproduction of the species being predated. The combined effect of these two processes enhances the nutrient cycling and fuels biomass productivity. By performing this activity, ciliates and flagellates increases their own biomass, attracting metazoan predators and functioning as linkage of lower and upper trophic levels in aquatic food webs [16, 35, 36].

The size of the ciliate determines the sizes of preys they can feed on. Thus, bacterivorous ciliates ingest a different particle size range; the preferred size spectrum for each species is a function to cytostome size and morphology. For example, small ciliates usually bacteria eat <3 μm [18, 37, 38]. Ciliates that feed on the smallest particles (<1 μm) require relatively high densities of these bacteria as a minimum to keep their population growth [30]. Several groups of ciliates actively feed on specific bacteria species for a period ranging between 44% and 100% of the time, because bacterial densities will have variations as responses to predation intensity along time [36].

Bacterivorous ciliates are present in all aquatic environments, from oligotrophic to eutrophic, in both freshwater and oceans. The diversity of bacterivorous ciliates and their contribution to the flow of energy in trophic networks depend on the dynamics of the systems in which they are living. Therefore, food resources are probably the main regulators of ciliated communities (diversity, abundance, and

biomass) [30]. For example, bacterivorous ciliates contribute very little for the direct transfer of bacterial production to the trophic networks of metazoans in oligotrophic environments. Ciliates consume less than 11% of bacterial productivity in these waters [39–41]. Perhaps the heterotrophic bacteria that are very small in these lagoons (0.035 to 0.4 μm) are grazed by bacterivorous ciliates at a very low rate [41], or the number of bacteria is not enough to support larger ciliate communities feeding on smaller bacteria (<1 μm), as they require high densities of bacteria to maintain their populations [30]. Then, productivity of oligotrophic systems function most of the time as bottom-up (availability of substrate and nutrients) controlled [42]. This functioning will remain until seasonal pulses of nutrients (or human subsidies) arrive, busting primary productivity and changing the system into top-down control, and it will keep functioning the same way until the pulse of nutrients (or subsidy) is completely metabolized, returning the system to the bottom-up dynamic.

Contrastingly, densities of heterotrophic bacteria in eutrophic environments are sufficiently higher to also keep a higher diversity of active bacterivores [43], fueling ciliates biomass productivity and allowing the intervention of metazoan predation. Top-down control (predation) seems to be in function all the time for regulating the abundance of heterotrophic bacteria in eutrophic systems [42]. Normally, communities of bacterivorous ciliates of small sizes (~ 30 μm) are found as dominant in eutrophic environments [30, 38]. The most abundant ciliates in these environments are small oligotrichs (*Halteria*), scuticociliates (*Cyclidium*), and Peritrichs (*Vorticella*) [30, 38, 44, 45]. *Halteria grandinella,* for example, is one of the most important bacterivores due to its high consumption rate of bacteria [38], the genus *Halteria* is very important in meso-eutrophic lakes because they prey on a large spectrum of sizes, from bacterial cell measuring just around 0.4 μm to up to 5 μm; they have a high potential growth rate, because of its efficient nutrient absorption, and show defensive strategies reducing their vulnerability to predation by metazooplankton in comparison to other common pelagic ciliates [45].

Sessile ciliates such as *Vorticella* and *Epistylis* are typical members of protists' community in aquatic environments [34, 45–49]. They heavily graze on bacteria having even higher ingestion rates than free-swimming bacterivorous protist and can account for 66% of total bacterivores. Even in small numbers, epibiotic ciliates can have a great grazing impact on bacteria [34]. For example, *Vorticellides aquadulcis* had the highest grazing rates of all the ciliates from a meso-oligotrophic lake community [38]. Some common bacterivorous ciliates are found in **Table 1**.

#### **2.3 Feeding on phototrophs**

There is a difficulty in assessing a proper name for the kind of food protists feed on when they become predators of phototrophs, as this group consists of both eukaryotic and procaryotic members, and neither of these primary producers may be considered as "plants" or "herbs". Feeding on them cannot be considered as herbivory. On the procaryotic part, cyanobacteria are a phylum comprising many species that, besides being phototrophs, can also produce toxic molecules, compromising the fresh water supplies for human consumption when growing unchecked in oligotrophic waters [50, 51]. From the eukaryotic part, there is an extra complication when trying to separate the permanent phototrophs from the mixotrophs.

Moving the sizes up, ciliates are one of the most important groups feeding on phytoplankton in marine and freshwater environments [18, 41, 52]. They may consume up to 74% of the daily phytoplankton production [53], becoming the key controllers of phytoplankton biomass [54]. On the other hand, ciliates mobilize the


#### **Table 1.**

*Trophic groups free-living ciliates in aquatic environments.*

highest proportion of organic carbon and nutrients in oligotrophic waters dominated by cyanobacteria, playing the fundamental role of linking the productivity of microbial food web with the metazoans [41, 53]. It has also been noticed that the flux of carbon up to metazoans is not interrupted when the density of bacterivores ciliates falls, but it is compensated by predation on ciliates feeding on phototrophs [41]. Some of the ciliates that feed on phototrophs are in **Table 1**.

Ciliates feeding on phototrophs represent between 30–65% of the total biomass of all functional groups of ciliates thriving in eutrophic lakes [55]. However, this dominance is not permanent. Ciliates feeding on phototrophs become very numerous on the blooming season [56], and even dominate the entire ciliate community for short periods between seasons [57].

Tintinnids tend to feed on small-cell-sized phytoplankton (2–20 μm) [58]. They are voracious phytoplankton feeders that may consume over half the quantity of these kind of phototrophs in marine waters [54] and over 69% of these primary producers in lakes [59]. Species like *Helicostomella subulata*, *Ptychocylis* spp., and *Parafavella* spp. make a significative contribution to biomass of ciliates feeding on phototrophs in marine environments [60].

Selective feeding has been observed in several species of ciliates. However, feeding on a wider spectrum of sizes and kind of phototrophs (non-selective feeding) allows them to take advantage of the productivity in hypereutrophic environments rich in small particulates [49]. The genus *Tintinnidium* groups species that dwell very well in these kinds of waters and may be used as model organisms to study the ciliates' adaptation to excess of organic matter [61].

#### **2.4 Predators of predators or raptorial feeders**

There are several species of ciliates and flagellates that feed on bacterivorous protists and on protists feeding on phototrophs. These are predators of predators. These predator species may feed temporarily on bacteria but cannot survive by just this consumption; they are attracted to them as they offer clues to discover their preferred preys: ciliates, flagellates, or amoebae feeding on bacteria.

Most of predator ciliates feed on preys around 10 times smaller than them [62, 63], although raptorial feeders may consume bigger preys, comparable to their own size or even bigger [64]. This capacity is due to their very flexible cytostome as is the case in protostomatids genera *Tiarina*, *Balanion,* and *Holophrya,* and in the litostomatid genus *Didinium* [62]. Ciliates select their food based on prey's size, motility, and biochemical composition of cells' surface [62]. Raptorial ciliates exert strong pressure on populations of small phototrophic and heterotrophic flagellates [65], imprinting some velocity to nutrient cycling in environments where productivity allows them to develop large populations.

Predatory ciliates are present in small numbers along seasons in oligotrophic waters, showing surges in population numbers, in synchrony with the increase of primary productivity during the spring, reaching up to 55% of the total ciliates' abundances in temperate waters [64, 66]. However, they only reach between 24.6% to 28.7% in freezing oligotrophic waters of the Arctic and Antarctic [67].

On the other hand, predatory ciliates become important top-down controllers of microbial food web productivity in eutrophic and hypertrophic waters [68]. Eutrophic waters have the conditions to sustain high productivity rates of phototrophs and heterotrophic bacteria, sustaining, in turn, large populations of their grazers, promoting the increase of predatory ciliate population [69]. Biomass of raptor ciliates may reach almost an order of magnitude higher in eutrophic compared to the one obtained in meso and oligotrophic lakes, suggesting that they are effectively controlling the primary productivity [70]. This assumption is supported by the covariance of predatory ciliates and their preferred food. For example, the increasing population of predatory ciliates bigger than 100 μm is related to a simultaneous shrinkage of abundance of smaller ciliates (<20–40 μm), mostly phototrophs and bacterivorous [71]. Big and voracious ciliate raptors like *Monodinium* sp. and *Lagynophrya* sp. have stronger impact than rotifers on populations of small ciliates [68]. However, quantity of prey is not the only important factor, and species diversity is needed to sustain more raptorial species of ciliates. For example, only *Monodinium* remained abundant when diversity of preys falls below a limit [72].

Several species of oligotrichs feed on bacterivorous flagellates, showing an efficiency of 45% biomass transformation, also fueling the bacterial productivity by releasing essential nutrients for heterotrophic bacteria to keep their population growth [65]. Some predatory ciliates are shown in **Table 1**.

#### **2.5 Omnivorous**

Omnivorous protists are an important group to look for when assessing the stability of a food web because their very presence means productivity is enough to non-specialists, to feed on a variety of resources. Omnivores strengthen the resilience of planktonic communities by regulating the trophic dynamics [73]. Omnivorous ciliates may have a preferred prey but can easily move to other kinds of prey, which may be more abundant or easier to catch [74]. This variety of resources for true omnivorous ranges from bacteria, algae, other ciliates of different sizes to fungi [73]. This versatility gives them an advantage to withstand a resource limitation by having alternative prey [70]. Additionally, omnivorous ciliates increase the stability of planktonic communities by feeding on species that may pass undetected from their specialized predators, by having densities small enough to get an advantage of the elimination of their competitors and increase their numbers. In this situation, omnivores would prevent them to reach high densities too fast, giving time for their specialized predators to increase to population levels that may effectively control the newly abundant prey.

#### *Food Webs DOI: http://dx.doi.org/10.5772/intechopen.97252*

Omnivorous ciliates are present in any kind of environment allowing the stability of protist communities. They are elements of marine and freshwater ecosystems, both oligotrophic [66, 75] and eutrophic [69, 76], as well as in polar waters [67].

As with the other trophic groups, omnivores show seasonal bursts of abundances in the communities they are part of, especially in oligotrophic waters where they are scarce most of the time, except for occasional bursts [77, 78]. Omnivorous ciliates are commonly found in lakes throughout the year, normally with low species richness, representing between 2–12% of the ciliates species [67, 79]. Their low contribution to the number of individuals makes them reach a peak of 35% during productivity bursts [66, 79]. However, this proportion may steadily increase in the proportion the environment is turning into the eutrophic condition, increasing the species richness, although the densities of omnivorous ciliates may momentarily diminish with the eutrophication [69] as result of the species increase (more species and lower number of individuals by species). Once the eutrophication reaches a steady state, the biomass of the omnivorous ciliates will reach high values and even dominate among ciliates [76].

The numbers of small omnivorous ciliates usually dominate in meso oligotrophic environments, feeding on dominant bacteria (<2 μm) and algae (2–20 μm) [49]. Food concentration is a very important factor, strongly affecting an easily detectable feeding behavior of omnivorous ciliates [73]. Several of the most common omnivorous ciliates are shown in **Table 1**.
