Influence of bacterial density and water temperature on the grazing activity of two freshwater ciliates

1. The influences of bacterial density and water temperature on the grazing activity of the ciliates Uronema sp. and Colpoda inflata were studied. The conditions assayed were two prey densities (10⁶ and 4 × 10⁷ bacteria ml^?1) and three water temperatures (10, 15 and 22 °C). 2. The response of the ciliates was measured from changes in protistan biovolumes and specific clearance rates. At high prey density, both ciliates showed lower biovolumes as water temperature increased, while at low prey density this tendency was minimized. 3. At the intermediate temperature of 15 °C both ciliates filtered ten times more body volume when bacteria were scarce; however, the ingested bacteria were fewer than at high prey density. At low prey density, a decrease from 15 to 10 °C evidenced different strategies of the two ciliates, which led to a similar ingestion of bacteria: C. inflata reduced its specific clearance rates and increased its biovolume, while Uronema sp. did not show changes. At high prey density, an increase from 15 to 22 °C caused lower biovolumes and a noticeable increase in specific clearance rates in both ciliates, indicating opportunist behaviour.     

Predation on ciliates by freshwater calanoid copepods: rates of predation and relative vulnerabilities of prey

• 1 The susceptibility of ciliates in a mesotrophic lake to predation by Epischura lacustris, Diaptomus minutus and D. pygmaeus was assessed during summer. Oligotrichs, particularly Strobilidium velox (c. 43 μm), were removed efficiently by adult copepods and contributed substantially to the diet of female D. minutus. The presence of approximately 1,6 adult Epischura 1-^?1, or sixteen adult female Diaptomus 1-^?1, could halt the growth of S. vechx populations in summer.
• 2 Factors affecting the rate at which copepods prey on ciliates were examined in experiments with D. pygmaeus and cultured ciliates. Rate of predation on S. velox, the preferred species, became saturated at 5 S. velox ml^?1 (45ngCml^?1) and did not change with a 10-fold increase in alternative algal food.
• 3 Behavioural differences among ciliates, and the presence of other ciliates, contributed to differences in ciliate susceptibility to predation and suggest reasons why rates of removal of ciliates are not related to ciliate size.
• 4 By feeding selectively, at high rates, calanoids may suppress populations of some ciliates and thereby influence microzooplankton community structure.

     

Intestinal ciliate composition found in the feces of the Turk rahvan horse Equus caballus, Linnaeus 1758

Species composition and distribution of large intestinal ciliates were investigated in the feces from 15 Turk rahvan horses, living in the vicinity of Izmir, Turkey. Twenty-two ciliate genera consisting of 36 species were identified. This is the first report on intestinal ciliates in Turk rahvan horses and no previously unknown species were observed. The mean number of ciliates was 14.2 ± 13.9 × 10⁴ cells ml⁻¹ of feces and the mean number of ciliate species per host was 9.9 ± 7.1. No ciliates were observed in 2 horses. Bundleia and Blepharocorys were considered to be the major genera since these ciliates were constantly found in high proportions. In contrast, Paraisotricha, Didesmis and Gassovskiella were only observed at low frequencies. The ciliates found in this survey had almost the same characteristics as those described in previous reports, suggesting that there was no significant geographic variation in the intestinal ciliate fauna of equids.     

The changes in the predatory behavior of the microturbellarian <Emphasis Type="Italic">Stenostomum sphagnetorum</Emphasis> on two species of toxin-secreting ciliates of the genus <Emphasis Type="Italic">Spirostomum</Emphasis>

It is known that the microturbellarian Stenostomum sphagnetorum, a common ciliate predator, is very sensitive against different types of toxins produced by other ciliates for chemical defense, and consequently, it is not able to capture and ingests these ciliates. In particular, when the predator tries to attack one of these toxin-secreting ciliates, it is forced to regurgitate the captured prey in response to the toxin discharged from the ciliates. In this study it is shown that after repeated attacks by S. sphagnetorum against two species of toxic ciliates (Spirostomum ambiguum and Spirostomum teres), the predator acquires a behavior of prey selection that leads to the exclusion of these ciliates among the possible prey and to the distinction between edible and inedible (toxic) ciliates. This learned behavior, which is maintained for days, is lost only after the asexual reproduction of the microturbellarian. In addition, S. sphagnetorum learns to recognize and avoid specimens of S. ambiguum and S. teres artificially deprived of their toxins, strongly suggesting that the toxins are not exclusively associated in the prey recognition of the microturbellarian.     

Monsoonal and lunar variability in microzooplankton abundance and community structure in the Terusan mangrove creek (Malaysia)

This study documents the monsoonal and lunar effects on species composition and abundance of microzooplankton in a tropical estuary. We investigated microzooplankton abundance in relation to the various environmental and biotic parameters, sampled in the Matang mangrove (Malaysia) from April 2013 to February 2014. A total of 39 microzooplankton taxa comprising four major groups, i.e. loricate ciliates (37.72%), aloricate ciliates (29.46%), dinoflagellates (24.33%) and meroplanktonic nauplii (8.49%) were identified. The loricate ciliates were the most diverse group with 31 taxa recorded. Four major species of loricate ciliates were identified, i.e. Tintinnopsis beroidea, Tintinnopsis rotundata, Stenosemella avellana and Tintinnidium primitivum, while Strombidiidae and Strobilidiidae dominated the aloricate ciliates. Although small loricate ciliates were ubiquitous, redundancy analysis shows marked shifts in microzooplankton community structure, from one that was dominated by loricate ciliates during the drier SW monsoon, to aloricate ciliates at the onset of the wet NE monsoon, and then to dinoflagellates towards the end of the drier NE monsoon period. These shifts were associated with rainfall, dissolved inorganic nutrients, salinity, temperature and microbial food abundance. There was no clear lunar effect on abundance of microzooplankton except for Favella ehrenbergii and copepod nauplii, which were more abundant during neap than spring tides.     

The role of predators in the stable coexistence of several alga species

Experiments were conducted on growing mixed cultures of green Ankistrodesmus arcuatus Korsch and diatom Diatoma elongatum (Lyngb.) algae with and without ciliates Cyclidium glaucoma Ehrenberg and Paramecium caudatum Ehrenberg in accumulative and perfusion cultures. Both alga species successfully developed in the presence of ciliates despite their grazing on both alga species; however, in their absence, Ankistrodesmus arcuatus were suppressed and did not develop. It is supposed that ciliates contribute to the stabilization of the community not only as predators but also by excreting dissolved reduced nitrogen into the environment as a result of their vital functions.     

Annual Changes of Abundance and Biomass of Planktonic Ciliates in the Gdańsk Basin,Southern Baltic

Seasonal changes in the species composition, abundance and biomass of planktonic ciliates were determined every 2–3 weeks at two sites of 30 m depth and one location of 105 m depth in the southwestern Gdańsk Basin between January 1987 and January 1988. A total of 40 ciliate taxa were observed during this period. Autotrophic Mesodinium rubrum dominated ciliate abundance and biomass: maximal values of 50 · 10⁻¹ ind. ^1-1 and 65 μg C 1⁻¹ were recorded. The annual mean biomass of M. rubrum comprised 6 to 9% of the annual mean phytoplankton biomass. The highest abundances and biomasses of heterotrophic ciliates were noted at all stations in the spring and summer in the euphotic zone with maximum values of 28 · 10³ ind. 1⁻¹ and 23 μg C 1⁻¹. Three ciliates assemblages were distinguished in the epipelagic layer: large and medium-size non-predatory ciliates, achieving peak abundance in spring and autumn; small-size microphagous ciliates and epibiotic ciliates which were abundant in summer, and large-size predacious ciliates dominating in spring. Below 60 m, a separate deep-water ciliate community composed of Prorodon-like ciliates and Metacystis spp. was found. The ciliate biomass in the 60–105 m layer was similar to the ciliate biomass in the euphotic zone. The heterotrophic ciliate community contributed 10 to 13% to the annual mean zooplankton biomass. The potential annual production of M. rubrum comprised 6 to 9% of the total primary production. Carbon demand of non-predatory ciliates, calculated on the basis of their potential production, was estimated to be equivalent to 12–15% of the gross primary production.     

Effects of marine ciliates on survivability of the first-feeding larval surgeonfish,Paracanthurus hepatus: laboratory rearing experiments

The contribution of ciliates as a food source to survival of first-feeding surgeonfish larvae, Paracanthurus hepatus, was examined in rearing experiments. The larvae were exposed to eight treatments; i.e. a tintinnid, Amphorellopsis acuta (1.0 × 10⁴, 5.1 × 10³ and 2.2 × 10³ cells l^–1) and a naked ciliate, Euplotes sp. (1.3 × 10⁴, 8.0 × 10³ and 5.0 × 10³ cells l^–1), plus two controls without ciliates. Highest survival of the larvae over the first 4–8 days was observed in the highest density of A. acuta. Rearing experiments also showed that the survivals of larvae fed with A. acuta were higher than those fed with Euplotes sp. Gut content analyses revealed loricae of A. acuta in the larvae. Although Euplotes sp. (lacking loricae) was never recognized in those larval guts, feeding on Euplotes sp. by larvae was confirmed using the ciliate labeled with fluorescent microspheres, implying that the feeding on naked ciliates by fish larvae has been overlooked. The results strongly suggested that both tintinnid and naked ciliates play important roles as alternative food sources to copepod nauplii by enhancing the survivability of fish larvae, especially those with a smaller mouth.     

Feeding by ciliates on two harmful algal bloom species, Prymnesium parvum and Prorocentrum minimum

We have focused on ciliates as potential grazers on toxic phytoplankton because they are major herbivores in aquatic food webs. Ciliates may exert top down control on toxic phytoplankton blooms, potentially suppressing or shortening the duration of harmful algal blooms (HABs). We measured the growth rates of several ciliate species on uni-algal and mixed diets of both HAB and non-HAB algae. The tintinnids Favella ehrenbergii, Eutintinnus pectinis and Metacylis angulata and the non-loricate ciliates Strombidinopsis sp. and Strombidium conicum were isolated from Long Island Sound (LIS), and fed HAB species including the prymnesiophyte Prymnesium parvum (strain 97-20-01) and the dinoflagellate Prorocentrum minimum (strains Exuv and JA 98-01). Ciliates were fed algal prey from cultures at various growth phases and at varying concentrations. We observed no harmful effects of P. minimum (Exuv) on any of the ciliates. However in a comparison of strains, P. minimum (Exuv) supported high growth rates, whereas P. minimum (JA 98-01) supported only nominal growth. P. parvum was acutely toxic to ciliates at high concentrations (2×10⁴–3×10⁴ cells ml⁻¹). At low concentrations (5×10³–1×10⁴ cells ml⁻¹), or in culture filtrate, ciliates survived for at least several hours. In mixed diet experiments, as long as a non-toxic alga was available, ciliates survived and at times grew well at concentrations of P. parvum (5×10²–3×10⁴ cells ml⁻¹) that would otherwise have killed them. The present study suggests that prior to the onset of toxicity and bloom formation ciliates may exert grazing pressure on these HAB species, potentially contributing to the suppression or decline of P. minimum and P. parvum blooms.     

Protozoan epibionts on Mysis relicta Loven, 1862 (Crustacea, Mysidacea) from Lake Lüšiai (Lithuania)

Protozoan epibionts were found on specimens of the mysid Mysis relicta collected in Lake Lü?iai (Lithuania). These protozoans belong to three genera of ciliates: Vorticella, Dendrosoma and Tokophrya, and were located on the antennae, carapace, appendages and abdomen of the basibiont. The ciliates of the genus Vorticella had a bell‐shaped body, with concave‐type striations and a very long contractile stalk. The stalk joined the body via a truncated and overlapping zone. The macronucleus was J‐shaped, and the contractile vacuole was anterolateral. Only one ciliate species of Vorticella has been found on mysids, although on species other than M. relicta, and this is therefore the first record of Vorticella on M. relicta, and the second on the order Mysidacea. The ciliates of the genus Dendrosoma had an irregular body directly attached to the substrate. Finger‐like actinophores arose from the body, with a bundle of tentacles at their ends. The macronucleus ramified into branches that followed the actinophores. These ciliates were included in the species D. astaci. The presence of this ciliate represents the first record of this genus on Mysis relicta. The ciliates of the genus Tokophrya had a pyramidal body, the apical surface of which showed two conspicuous actinophores, with a short, longitudinally striated stalk joining to the body via a narrow unstriated band. The macronucleus was spherical or ovoid, centrally located, and there was an apical contractile vacuole. Only one previous study has referred to the presence of this genus on Mysis relicta, and the data contained in it were compared with those of the present study. The biometrical data and taxonomical position of the ciliate epibionts was considered.     

The ciliated protozoa of the monomictic Lake Kinneret (Israel): species composition and distribution during stratification

The ciliate taxa from epilimnion, hypolimnion, and littoral of Lake Kinneret were studied from November to December 1987 during stratification. Two collections of planktonic and benthic ciliates were taken at each of six sampling stations. Benthic ciliates from the littoral zone were collected at seven stations along the lake shore. Densities were determined for each ciliate species and for total protozoans at each station and sampling date. Thirty-six species of ciliates, representing 31 Genera, 18 Orders and 7 Classes, were identified. Planktonic protozoans characteristic of the epilimnion included Coleps hirtus and Vorticella mayeri. The more abundant taxa of benthic ciliates in the profundal of the lake included Saprodinium dentatum, Plagiopyla nasuta and Dexiotricha plagia. The predominant ciliate in the littoral was Pleuronema coronatum. Principal component analysis, performed on the correlation matrix of both sampling stations and species, revealed that epilimnion, hypolimnion, and littoral belt were colonized by different ciliate communities.     

Sterol Composition of Freshwater Algivorous Ciliates Does Not Resemble Dietary Composition

Algivorous ciliates represent an important link in freshwater food webs, as they transfer energy and biochemical matter from their algal prey to mesozooplankton predators. However, it is still unknown how dietary composition influences the biochemical composition of ciliates. We analyzed the sterol composition of the algivorous ciliates Balanion planctonicum and Urotricha farcta and compared it to the sterol composition of their diet—the cryptomonad Cryptomonas phaseolus. The sterol composition of the ciliates did not resemble that of their algal diet. Ergosterol [(22E)-ergosta-5,7,22-trien-3β-ol] was the sterol in highest concentration in C. phaseolus, whereas stigmasterol [(24S)-24-ethylcholesta-5,22E-dien-3β-ol] was dominant in both B. planctonicum and U. farcta. Moreover, the occasionally higher sterol concentrations in the ciliates than in their algal diet suggest sterol accumulation by the ciliates. We conclude that dietary sterol composition influences the composition of the two algivorous ciliates studied, but species-specific differences in metabolism probably determine the ultimate sterol composition of the ciliates.     

Trophic coupling of the microbial and the classical food web in Lake Baikal,Siberia

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Susceptibilities of different-sized ciliates to direct suppression by small and large cladocerans

• 1 Laboratory experiments compared the susceptibilities of six ciliates and the rotifer Keratella cochlearis to predation and interference from Daphnia pulex and Bosmina longirostris.
• 2 Susceptibilities of the ciliates to D. pulex were similar to or less than that of the rotifer, and decreased with increasing ciliate size. Most ciliates were just as susceptible to B. longirostris as to the much larger D. pulex. The jumping response of the oligotrich Strobilidium gyrans appeared to be an effective defence against B. longirostris.
• 3 Clearance rates of B. longirostris and D. pulex on different ciliate species at a density of 1,3 ciliates ml^?1 ranged from 1–30 to 5–24ml ind.^?1 day^?1, respectively. In natural plankton communities, cladocerans could impose high mortality rates on ciliates and shift the size structure of ciliate assemblages towards larger and less susceptible species.

     

Monoxenic culture of the anaerobic ciliate Trimyema compressum Lackey

Sapropelic ciliates from anoxic mud samples were enriched and cultivated in monoculture together with natural food bacteria growing on cellulose. The ciliates lacked cytochrome oxidase and contained bluish fluorescent endosymbionts. One of the anaerobic ciliates, Trimyema compressum, contained methanogenic bacteria as was shown by methane formation. During continued cultivation, T. compressum gradually lost its endosymbionts. With SEM microscopy no episymbiotic bacteria could be detected.From enrichment cultures of T. compressum, anaerobic bacteria were isolated in pure culture. One of the strains, a Bacteroides spec., proved capable of serving as food bacteria, thus allowing establishment of monoxenic T. compressum cultures. These cultures exhibited a requirement for sterols as growth factors. The doubling time of this ciliate was 13 h at 28°C. The highest yield obtained was 2100 cells/ml.Dedicated to Holger W. Jannasch on the occasion of his 60th birthday     

Syndinean dinoflagellates of the genus Euduboscquella are paraphyletic

Syndinean dinoflagellates of the genus Euduboscquella infect marine ciliates and dinoflagellates. Euduboscquella species infecting dinoflagellates are understudied relative to congeners infecting ciliates and their molecular phylogeny remains uncertain. Morphology, development, and rRNA gene sequences of intracellular parasites infecting heterotrophic dinoflagellates from coastal waters of Busan, Republic of Korea in summer to fall of 2019–2021 indicate that Cucumeridinium coeruleum, Gyrodinium cf. ochraceum, and two unidentified species of Gyrodinium were each infected by a different Euduboscquella species. Morphological features including shield structure, shape and color of the mature trophont, and sporogenic process distinguished each of the four parasites from the 10 previously described species of Euduboscquella. Our molecular and phylogenetic analyses showed considerably greater genetic distance of SSU and ITS-LSU rRNA gene regions among Euduboscquella species infecting dinoflagellates than among those infecting ciliates. Rather than clustering as a group with Euduboscquella species infecting ciliates, SSU rRNA sequences of the four novel parasites spread out across the syndinean Group I phylogeny, occurring in two different clades and a new lineage. Placement of our novel parasites in multiple clades that encompass Ichythyodinium chabelardi strongly indicates that the genus Euduboscquella is paraphyletic.     

Abundance and Community Structure of Picoplankton and Protists in the Microbial Food Web of Barguzin Bay,Lake Baikal

We examined the vertical abundance of bacteria, phytoplankton and protists along a transect of six stations from near-shore (Stn. 1) to off-shore (Stn. 6) in Barguzin Bay of Lake Baikal, in the summer of 2002. Chlorophyll concentrations at Stn. 1 were higher (>10μg l⁻¹) than at the other five stations (<3μg l⁻¹). Planktonic and sessile diatoms dominated at Stn. 1, while pico-phytoplankon was dominant at other stations. Densities of heterotrophic bacteria were high in both the epilimnion and the thermocline at all stations. Nanoflagellates were abundant in the epilimnion, and ciliates in the thermocline, but no horizontal trend could be found for these heterotrophs. At Stn. 1, not only filter feeding (Strombidium and Strobilidium) and raptorial (Balanion) ciliates but also predatory ciliates (Prorodon and Spathidiosus) dominated, while at other stations only the filter feeding and raptorial ciliates were dominant. In off-shore stations (Stns. 5 and 6), significant correlations were detected between concentrations of chlorophyll a and density of filter feeding or raptorial ciliates, suggesting tight food linkages between phytoplankton and these ciliates. The concentration of dissolved organic carbon (DOC) was significantly correlated with chlorophyll a concentration, although there was no significant correlation between DOC concentration and bacterial density. We suggest that there is a shift of the dominant food linkage from a herbivorous food chain in near-shore areas to a microbial food web in off-shore areas in Barguzin Bay of Lake Baikal.     

The effects of saprobic conditions on some ciliated Protozoa in the benthos and hypolimnion of a eutrophic pond

Seasonal fluctuations in numbers of some mesosaprobic ciliated Protozoa were followed from May 1969 to December 1970 in a eutrophic pond in north-west England. The most common species were Loxodes magnus and Loxodcs striatus; some counts of Frontonia leucas, Spirostomum teres, Stentor coeruleus and Paramecium caudatum were also made. From about October to May, when the pond was mixed and the bottom water was well oxygenated, dense benthic populations of these ciliates were found (maxima 221 L. magnus and 293 L. striatus in 0·1 ml of sediment). They were absent from the plankton. In summer, stratification occurred, conditions in the hypolimnion became saprobic (i.e. low oxygen and high levels of potentially toxic substances such as sulphide, ammonia, and carbon dioxide), and very few benthic ciliates were present. Some planktonic Loxodes (up to 34 L. magnus and 137 L. striatus/ml) were, however, found in the hypolimnion. Possibly conditions in the water column were less severe than in the sediment, or perhaps the planktonic ciliates migrated vertically, from time to time, to an oxygen supply at the boundary with the epilimnion. Experimental exposure of the Loxodes species (also S. teres) to saprobic conditions in closed bottles caused the death of most ciliates within 50–150 h of closing the bottles. Deoxygenation of Loxodes was also carried out in a stream of argon, when there was no build-up of the potential toxins associated with anoxia. Almost all Loxodes were lost between 20 and 70 h, hence, oxygen deficiency alone is probably sufficient to explain the low populations in the summer benthos.     

Cyclopoids feed selectively on free-living stages of parasites

1. Many aquatic organisms can consume parasite larvae, thus hampering parasite transmission; however, information about feeding on them in the presence of an alternative prey remains scarce. When having a food choice, predators may decrease parasite consumption, therefore, it is important to assess the role of parasites in the diet of predators in natural communities with different types of prey available. Our study aims to test whether common freshwater cyclopoids feed on trematode free-living stages (cercariae) when an alternative food source is present.
2. We experimentally studied ingestion rates of cyclopoids Macrocyclops distinctus fed with cercariae of trematode Diplostomum pseudospathaceum, a common and harmful parasite of freshwater fishes, and ciliates Paramecium caudatum (an alternative prey, known as suitable food for copepods). First, the feeding response of cyclopoids to different densities of each prey was studied. Then, feeding selectivity in the mixtures of cercariae and ciliates was tested.
3. Feeding rates of cyclopoids increased with prey densities (both ciliates and cercariae) but almost stopped growing at high prey densities, which indicated saturation (Holling type II functional response). In most cases, cyclopoids consumed cercariae at higher rates than ciliates. Maximum ingestion rates estimated from the obtained curves were 37 cercariae ind⁻¹ hr⁻¹ and 17 ciliate ind⁻¹ hr⁻¹.
4. When exposed to prey mixtures, cyclopoids fed on cercariae selectively. When cercariae were offered to cyclopoids at concentrations exceeding the saturation level, the ingestion of ciliates remained constantly low at all ciliate densities. In contrast, the ingestion of cercariae increased with rising cercariae densities even when ciliates were presented ad libitum, decreasing only at very high prey densities. Possible reasons of such feeding preferences are discussed.
5. Our study demonstrated that cyclopoids may prefer to feed on cercariae when there is an alternative food choice and can ingest cercariae at high rates. These experimental results could be extended to natural communities, suggesting that cyclopoids can reduce the transmission of parasites and contribute to the incorporation of parasite production in food webs of lentic ecosystems.

     

Genetic analysis of ciliates living on the groundwater amphipod Crangonyx islandicus (Amphipoda: Crangonyctidae)

Two endemic subterranean freshwater amphipod species have been discovered in groundwater of the volcanic active zone in Iceland, Crangonyx islandicus and Crymostygius thingvallensis. At least five different ciliate sequences were isolated from C. islandicus and the analysis of variation at the 18S ribosomal DNA gene suggests that they present previously unsequenced species, from the orders Apostomatida and Philasterida. Apostome ciliates are well known to be exuviotrophic epibionts on crustaceans. Analyses of ciliate epibionts from different groundwater amphipod species from North America and mainland Europe revealed distinct groups of ciliates and higher diversity on the epigean amphipod Crangonyx pseudogracilis. Analysis of geographic patterns of the most common ciliate within Iceland revealed population differentiation supporting limited current connectivity between the different groundwater systems. Our study reports an occurrence of previously undescribed ciliate species in a groundwater ecosystem characterized by low species diversity.