The ecology of two species of primitive ciliated protozoa commonly found in standing freshwaters (Loxodes magnus stokes and L. striatus penard)

The distribution of Loxodes magnus and L. striatus (Karyorelictida) was investigated in two eutrophic waters (Esthwaite Water and Priest Pot, English Lake District). In the benthos, these species were most abundant at the sediment surface, at deeper sites, and when the bottom water was oxygenated. In the plankton, in Priest Pot, they were found only in the oxygen deficient summer hypolimnion. Experimental studies suggested that L. magnus and L. striatus required access to oxygen. Loxodes was apparently excluded from the oxygenated Priest Pot epilimnion by several adverse factors, one of which was bright light. It was concluded that the ecology of L. magnus and L. striatus resembles, in many ways, that of the advanced ciliates which were found associated with Loxodes.     

The vertical distribution of some ciliated Protozoa in the plankton of a eutrophic pond during summer stratification

The vertical distribution of some ciliated Protozoa in the plankton of a pond in north-west England was investigated during August 1971. At this time, when the pond was stratified with an oxygen dificient hypolimnion, ciliates were counted at 10-cm depth intervals every 5 h over 25 h. The most common species (Loxodes magnus and L. striatus) were confined to the hypolimnion; there was no diurnal migration into the epilimnion. Earlier work had shown that Loxodes species require oxygen; it is therefore possible that these ciliates, which inhabited the oxygen dificient hypolimnion, migratedvertically, from time to time, to an oxygen supply at the boundary with the well-oxygenated epilimnion. To test this, Loxodes populations were confined in cellophane tubese both in the hypolimnion (at 3 m) and epilimnion (0.5 m) for 12 and 24 h (earlier trials had shown that the tubes were not markedly toxic). The ciliates died at both depths, and in a further experiment when Loxodes were confined at 3 m and 0.5 m and sampled at 5-h intervals up to 25 h it was found that they survived longer in the hypolimnion. It is suggested that ciliatees confined at 3 m died because they were unable to migrate vertically to an oxygen supply, while those at 0.5 m died because some other adverse factor was operating in the eiplimnion. Laboratory experiments showed that Loxodes died inn water in which phytoplankton photosynthesis took place and it is suggested that side effects of photosynthesis in the epilimnion (e.g. a rise in pH) caused the death of ciliates exposed at 0.5 m.     

The effects of photosynthetically raised pH and light on some ciliated Protozoa in a eutrophic pond

Some ciliated Protozoa (e.g. Loxodes magnus, L. striatus, Spirostomum teres, S. ambiguum and Frontonia leucas) are abundant during summer in the hypolimnion of a eutrophic pond in north-west England but are absent from the epilimnion. The work described in this paper was begun with the aim of investigating the suggestion that high pH values caused by phytoplankton photosynthesis contributed to the exclusion of these ciliates from the epilimnion. In July 1973, phytoplankton photosynthesis and high pH were found only in the epilimnion, hence conditions were compatible with the above suggestion. Ciliates were, therefore, kept in the laboratory in hypolimnion water and were exposed to phytoplankton photosynthesis, both with and without pH increase. It was found that Loxodes died under both treatments hence there is no evidence that high pH is lethal to Loxodes. It seemed possible, therefore, that either light or toxins released by algae during photosynthesis are lethal to Loxodes. L. magnus was, therefore, exposed to light in the absence of phytoplankton (in filtered hypolimnion water) both in the laboratory and in the pond and it was found that light was lethal. High light intensities might, therefore, contribute to the exclusion of at least Loxodes species from the surface water of the pond, although other adverse factors are probably operative since Loxodes species do not migrate into the epilimnion at night.     

Observations over 24 hours on the quantity of algae inside grazing ciliated protozoa

Summary The numbers of cells of the alga Scenedesmus (S. quadricauda and S. denticulatus) inside natural populations of grazing ciliated protozoa from a eutrophic pond (Loxodes magnus and L. striatus) were counted at 4 h intervals over two 24 h periods. There were no diel fluctuations in number of algal cells inside the protozoa, therefore the grazing rates were probably more or less constant over 24 h. L. magnus contained more algae than the smaller L. striatus. S. quadricauda was the more abundant Scenedesmus species in the phytoplankton and both Loxodes species contained more S. quadricauda than S. denticulatus, although the ratio S. denticulatus cells/S. quadricauda cells was greater inside the ciliates than in the phytoplankton.     

The hypolimnetic protozoan plankton of a eutrophic lake

The seasonal distribution of benthic species in the water column above and below the thermocline in a small eutrophic lake is described. During summer stratification populations of Spirostomum spp, Loxodes spp., Plagiopyla and Deltopylum become established in the plankton on or below the oxycline/thermocline. At shallow sites no migration occurred and populations of the migratory species in the benthos were sparse, with the exception of Plagiopyla which occurred in high densities in the sediment. Two distinct planktonic populations are established during stratification: an epilimnetic community of obligate planktonic ciliates and a hypolimnetic community of benthic migrants.     

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.     

Vertical distribution of planktonic ciliates in strongly stratified temperate lakes

The vertical distribution of planktonic ciliates in eight strongly stratified temperate lakes was studied in summer 1998. Ciliate abundance and biomass were highest (mean 39.9 cells ml^–1 and 181.9 g C l^–1) in the epi-, and lowest (mean 8.2 cells ml^–1 and 97.6 g C l^–1) in the hypolimnion. The community of ciliates was dominated by five orders: Oligotrichida, Haptorida, Prostomatida, Scuticociliatida and Peritrichida. The community composition varied greatly with depth. In the epilimnion, the ciliate numbers were dominated by oligotrichs but small algivorous prostomatids, peritrichs and haptorids were also numerous. In the metalimnion, these groups were replaced by scuticociliates and mixotrophic prostomatids. In the hypolimnion species known as benthic migrants appeared. We found a positive significant correlation (p < 0.05) between ciliate numbers and Chl a and bacterial densities. Only in the hypolimnion, the correlation between ciliates numbers and Chl a was not significant.     

Vertical and Seasonal Dynamics of Planktonic Ciliates in a Strongly Stratified Hypertrophic Lake

Seasonal population dynamics and the vertical distribution of planktonic ciliates in a hypertrophic and strongly stratified temperate lake were studied from April to October in 2000 and from April to June in 2001. In the epi- and metalimnion the ciliate abundance peaked in spring and late summer, reaching maximum values in the metalimnion (86 cells ml⁻¹) on 7th August 2000. In the epilimnion, the highest biomass content (414 μg C l⁻¹) was observed on 8th May 2000. In the hypolimnion only a late summer peak occurred and the ciliate numbers were always lower than in the epi- and metalimnion. Five groups dominated the community of ciliates: Oligotrichida, Gymnostomatea, Prostomatida, Hymenostomata and Peritrichia, and the community composition varied greatly with depth. In the epilimnion the ciliate numbers were dominated by oligotrichs but small algivorous prostomatids, peritrichs and gymnostomes were also numerous. In the metalimnion these groups were gradually replaced by scuticociliates and mixotrophic Coleps spp. In the hypolimnion scuticociliates and species known as benthic migrants dominated. In the epilimnion and upper metalimnion in spring large herbivores and in summer small bacterivores were more numerous.     

Morphology and Phylogeny of Two Species of Loxodes (Ciliophora,Karyorelictea), with Description of a New Subspecies,Loxodes striatus orientalis subsp. n.

The morphology and phylogeny of Loxodes vorax and L. striatus orientalis subsp. n. were investigated based on infraciliature and small subunit (SSU) rRNA gene sequence data. Loxodes striatus orientalis subsp. n. was separated from L. striatus striatus stat. n. by having fewer dikinetids in the intrabuccal kinety (35–55 vs. 50–70) and a variable number of macronuclei (2–4 vs. 2). In addition, the SSU rRNA gene sequence of the new subspecies differs in 13 and 11 nucleotides from that of two populations of the nominotypic subspecies. We also summarized the morphological differences between Loxodes and Remanella based on the data available. Phylogenetic analyses revealed that the genus Loxodes was monophyletic and nested within Remanella species. This study might, therefore, support the hypothesis that the freshwater genus Loxodes evolved from the marine genus Remanella.     

Nitrate respiration by Protozoa (Loxodes spp.) in the hypolimnetic nitrite maximum of a productive freshwater pond

SUMMARY.

• 1 The ciliated protozoon Loxodes dominated the microfaunal community living in the anoxic hypolimnion of Priest Pot, a small productive pond. Its peak abundance close to the oxic-anoxic boundary was always associated with a peak in nitrite (NO₂) concentration. Both peaks were usually found in water containing μ1 μmol O₂ 1^-1.
• 2 The microfauna were concentrated on a 30 μim sieve. The number of Loxodes in the sieve retentate correlated well with the activity of nitrate reductase in the same material, implying that the enzyme was located in Loxodes. It is unlikely that residual bacterial contamination could have accounted for the activity.
• 3 A doubling of specific electron transport system activity was associated with the transition across the oxic–anoxic boundary. This is consistent with the switch to nitrate respiration and the lower energy yield it provides.
• 4 Dissimilatory nitrate reduction was deduced to be the source of the nitrite peak. Nitrate was supplied by both run-off and nitrification.
• 5 It is suggested that Loxodes participates in the dissimilatory sequence of a condensed nitrogen cycle functioning across the oxic—anoxic boundary.

     

Temporal and vertical distribution of ciliophoran communities in the benthos of a small eutrophic loch with particular reference to the redox profile

SUMMARY. The ciliate communities occurring at three benthic sites in a small eutrophic loch have heen investigated over a 2-year period. Two characteristics of the community were studied in detail, the pattern of vertical distribution within the sediment and the temporal distribution of ciliates occurring in the surface sediment. The relationships between ciliate distributions and the environmental factors recorded were analysed by multiple regression. Significant relationships were revealed between vertical distribution of ciliates and the sediment redox (Eh) profile, the larger ciliate communities being associated with regions of higher potential. Other factors such as sediment density, organic matter, temperature and daylength, combined with other indicators of benthic metabolism (sulphide ion activity (Es^2?), pH, oxygen flux) were selected in the regression analysis as accounting for much of the variation in the depth distribution of ciliates. In analysing the temporal distribution of ciliates in the surface sediment, numbers were inversely related to Eh, Es^2? and oxygen flux, a result of the upwards migration of reducing conditions and greater microbial activity in the sediment surface during the summer. Daylength, temperature, organic carbon and benthic chlorophyll-a were also selected as accounting for much of the variation in ciliate number. It is proposed that the large increases in number and biomass of surface-sediment cilates in the summer months resulted from an intolerance of reducing conditions developing immediately beneath the surface and the increased productivity of the benthos as a whole during this period. Methods are also described for the construction, calibration and operation of electrodes used in measuring Eh, Es^2? and oxygen flux in the freshwater benthos. Data recorded for these three variables revealed similar seasonal patterns at each site in each of two consecutive years.     

Fish interactions with the sediment-water interface

In two mesocosm experiments of cross-classified design, using sixteen 900-liter containers, we measured how benthivorous, omnivorous, and planktivorous fish interact with the sediment-water interface to influence planktonic and benthic production. Experiment 1 used three fish treatments (Ictalurus punctatus, Notemigonus crysoleucas, Lepomis macrochirus) and a fishless control in the presence or absence of a natural pond sediment layer. The benthivorous Ictalurus enhanced turbidity but had no effects on dissolved oxygen, diel changes in dissolved oxygen, pH, or nutrient concentrations. All parameters measured were unaffected by the planktivorous Notemigonus. Experiment 2 compared Ictalurus nebulosus with those of other benthivorous (Cyprinus carpio) and omnivorous (Dorosoma cepedianum) fish, again in the presence or absence of a sediment layer but at a higher stocking density than experiment 1. In the second experiment, Dorosoma enhanced dissolved oxygen levels but had no effect on turbidity while Cyprinus and Ictalurus enhanced turbidity but suppressed dissolved oxygen. Nitrogen concentrations in sediment tubs were enhanced by Cyprinus and Ictalurus but nitrogen concentrations in sediment-free tubs were enhanced by Dorosoma. This would suggest that the benthivores affected nutrient levels through resuspension of sediments while omnivores affected nutrient levels through physiological processes.     

Seasonal development of hypolimnetic ciliate communities in a eutrophic pond

Abstract The ciliated protozoan communities in the hypolimnion of a highly produtive pond were investigated over two years. Three physiological groups could be distinguished: stratified water column; (b) anaerobic ciliates with endosymbiotic methanogens; and (c) anaerobes without endosymbiotic methanogens. Both groups of anaerobes were confined to the anoxic zone of the hypolimnion. Community biomass was dominated by microaerobic ciliates which had on average 20 times larger cells than anaerobic ciliates. Abundance and biomass of microaerobic ciliates decreased over the summer, while anaerobic ciliates increased. This reflected a spatial shift in the availability of inorganic nutrients and, as a result, of ciliate food from the epi- and metalimnion to the hypolimnion. The low biomass production of anaerobic ciliates was consistent with the low theoretical growth efficiency of anaerobic metabolism. Ciliate species displayed characteristic spatial and seasonal distribution patterns within the water column which were similar in both years investigated. Spatial and temporal distribution was mainly governed by two factors: (1) the distribution of dissolved oxygen; and (2) the availability of food. Distribution patterns were not related to chemical gradients other than the oxygen gradient, but they were correlated with the distribution of major food sources.     

Nitrate Accumulation in Aerobic Hypolimnia: Relative Importance of Benthic and Planktonic Nitrifiers in an Oligotrophic Lake

Both nitrate and nitrous oxide accumulate in the hypolimnion of the oligotrophic Lake Taupo, New Zealand, throughout stratification. The two forms of oxidized nitrogen increase in concentration with increasing depth toward the sediments, where the dissolved concentrations of reduced nitrogen are two orders of magnitude higher than concentrations in the overlying water. Nitrification rates were measured by dark [¹⁴C]CO₂ assays with and without the inhibitor nitrapyrin. The fastest rates were recorded for planktonic nitrifiers in the epilimnion and benthic species in the surficial 2.5 mm of the sediments. Nitrifying bacteria were least active in the deep hypolimnion. Deepwater accumulation of NO₃⁻ in Lake Taupo must therefore be a product of benthic rather than planktonic nitrification.     

Genetic diversity along the life cycle of the cyanobacterium Microcystis: highlight on the complexity of benthic and planktonic interactions

Microcystis is a toxic freshwater cyanobacterium with an annual life cycle characterized by the alternation of a planktonic proliferation stage in summer and a benthic resting stage in winter. Given the importance of both stages for the development and the survival of the population, we investigated the genotypic composition of the planktonic and benthic Microcystis subpopulations from the Grangent reservoir (France) during two distinct proliferation periods. Our results showed a succession of different dominant genotypes in the sediment as well as in the water all along the study periods with some common genotypes to both compartments. Analysis of molecular variance and UniFrac analysis confirmed the similarity between some benthic and planktonic samples, thus evidencing exchanges of genotypes between water and sediment. Thanks to these data, recruitment and sedimentation were proven not to be restricted to spring and autumn, contrary to what was previously thought. Finally, genetic diversity was significantly higher in the sediment than in the water (P < 0.01; Student's t‐test). Taken together, our results shed light on the hidden contribution of the benthic compartment in maintaining the genetic diversity of Microcystis populations throughout their annual cycle, which could explain their ecological success in aquatic ecosystems.     

Benthic–pelagic coupling: a comparison of the community structure of benthic and planktonic heterotrophic protists in shallow inlets of the southern Baltic

1. The taxonomic composition, abundance and biomass of heterotrophic protists (ciliates, heterotrophic flagellates (HF), rhizopods and actinopods) in the sediment and water column of shallow inlets of the Southern Baltic was studied under a variety of environmental conditions during 1996–1997. A shallow, highly eutrophic station and a deeper, less eutrophic station were compared.
2. Community biomass ranged from 0.12 to 0.34 μg C cm?3 in the water column and from 1.5 to 105 μg C cm?3 in the sediment. Heterotrophic protists dominated zooplankton biomass at both stations (73% and 84% mean contribution), while they were of minor importance within the zoobenthos. Expressed per unit area, benthic biomass contributed a significant part (44% and 49%) to the total heterotrophic protistan community at both stations.
3. Although the methodology for counting ciliates and HF was focussed on a high taxonomic resolution, the results reveal some general trends in the distribution of heterotrophic protists: protozooplankton biomass was dominated by flagellates (80% mean biomass contribution) at the shallow station and by ciliates (73% mean biomass contribution) at the deep station. In the benthos at both stations, ciliates were the dominant protozoans, followed by the hitherto little‐studied rhizopods (25% and 35% mean biomass contribution) and flagellates.
4. The degree of benthic–pelagic coupling differed between taxonomic groups. Benthic and pelagic communities of ciliates showed little taxonomic overlap. In contrast, many heterotrophic flagellate species were found both in the benthos and in the pelagic. These benthic–pelagic species contributed significantly to the biomass of HF in the water column. The planktonic rhizopod community consisted of a subset of those species found in the benthos.
5. The abundance of benthic and pelagic protists was positively correlated at the shallow station, but taxonomic data indicate that the direct exchange between benthic and pelagic communities was only partly responsible.     

Interstitial Ciliates: Benthic Microaerophiles or Planktonic Anaerobes?

We observed marine benthic interstitial ciliates Geleia sp. and Tracheloraphis sp. inhabiting the water column of a chemically stratified salt pond. This habitat is uncharacteristic for interstitial ciliates, yet they displayed active and abundant planktonic populations (up to 800 and 250 cells/liter, respectively) and a well-defined pattern of vertical distribution. Completely absent from the oxygenated epilimnion, they first appeared at the oxic/anoxic interface and were present throughout the anoxic hypolimnion. The data could not be explained by a passive removal (e.g. by currents) of these ciliates from their conventional habitat (soft sediments) to water column. The results suggest that 1) these ciliates favored an anoxic environment, and 2) they switched to a planktonic lifestyle as appropriate conditions (seasonal anoxia) developed in the water column. This sharply contrasts the classic view of these ciliates as specifically benthic and aerobic (albeit microaerophilic) organisms. We hypothesize that Geleia sp. and Tracheloraphis sp. can readily grow in either water column or benthos, but are typically found in sediments simply because they contain their preferred (anoxic) niche.     

Studies on ciliated protozoa in eutrophic lakes: 2. Field and laboratory studies on the effects of oxygen and other chemical gradients on ciliate distribution

An investigation into the spatial distribution of hypolimnetic ciliates in three small eutrophic lakes during the period of summer stratification was carried out. Peak ciliate densities were found to occur at the oxic/anoxic boundary, ciliate numbers declining with increasing depth within the hypolimnion. The ciliates only occurred in aerobic water where oxygen levels were less than about 0.5 mgl^–1 Laboratory experiments demonstrated that the ciliates swim upwards under anaerobic conditions but swim rapidly downwards under aerobic conditions. Further laboratory experiments showed that although the bulk of the population occured within anaerobic water, the hypolimnetic ciliates are aerobes and cannot survive indefinite anoxia. Despite the demonstrable toxicity of high levels of ammonia and sulphide, it was probably excesive distance from an available source of oxygen that excluded the ciliates from the lowest levels of the hypolimnion. Possible mechanisms which allowed these aerobic ciliates to colonise anaerobic water are considered.     

The behavioural responses and tolerance of freshwater benthic cyclopoid copepods to hypoxia and anoxia

The response of four benthic cyclopoid copepods,Acanthocyclops viridis (Megacyclops viridis) (Jurine, 1820),Macrocyclops albidus (Jurine),Eucyclops agilis (Koch, Sars) (Eucyclops serrulatus) (Fischer, 1851) andParacyclops fimbriatus (Fischer), to hypoxia and anoxia was investigated. All of these species died within six hours when confronted by totally anoxic conditions, but all survived four days at oxygen saturation levels as low as 25%. Males succumbed to the effects of anoxia more rapidly than the larger females of each species, and larger species survived for shorter periods than smaller species. In artificially stratified columns, where the lower layer was anoxic, all four species displayed an upward migratory response towards oxygenated conditions. Where the artificial hypolimnion was hypoxic, however, the migratory response was not observed. The results suggest that some benthic copepods cope with seasonal anoxia in eutrophic stratified lakes by migration rather than the various physiological adaptations shown by planktonic and semi-planktonic species.     

Dynamics and metabolic activity of the benthic cyanobacterium Microcystis aeruginosa in the Grangent reservoir (France)

The dynamics of benthic colonies of Microcystis aeruginosa (cyanobacteria)play an important part in the formation of the summer bloomunderlying many harmful effects. Because this benthic phaseremains somewhat unknown, we developed an approach using flowcytometry to follow the esterase activity of this species inthe Grangent reservoir. The esterase activity of benthic cyanobacteriaextracted from two layers of sediment (0–2 cm and 2–4cm deep) was measured weekly, as an indicator of viability,by flow cytometry with carboxyfluorescein diacetate. In parallel,the concentration of benthic cyanobacteria was estimated underepifluorescence microscopy and the water temperature and dissolvedoxygen concentration were measured in the hypolimnion. Esteraseactivity increased gradually as spring temperatures increased.This metabolic reactivation allowed one part of the benthiccyanobacteria to regain the water column, entailing a simultaneousdecrease of their number in the upper sediment (0–2 cm).Then, after a maximum in summer, esterase activity decreasedwhile the number of colonies increased. This corresponded withthe domination of the senescent planktonic form following thedecline of the bloom.