Feeding response of a benthic copepod to ciliate prey type,prey concentration and habitat complexity

1. Protozoans are important consumers within microbial food webs and, in turn, they represent potential prey for small metazoans. However, feeding interactions within these food webs are rarely characterised and this is especially true for freshwater sediments. 2. We aimed to quantify the feeding links between a freshwater meiofaunal copepod and ciliates in two laboratory experiments. The first experiment addressed the response of Eucyclops serrulatus towards ciliate density and type (two ciliate species of the same genus differing in terms of body size). A second experiment assessed the effect of habitat structure on feeding rates by introducing different structural complexity into the feeding arena. In contrast to the first experiment, which was run only for one time period, this experiment also tested three different total feeding times (4, 7 and 9 h). 3. Eucyclops serrulatus exhibited high ingestion rates, with 3–69 ciliates copepod^?1 h^?1 consumed depending on food concentration, food type and habitat complexity. Copepods exhibited a preference for the smaller ciliate when total ciliate concentration was low, but selected both ciliates equally when food concentrations were medium or high. However, at very high food concentration, Eucyclops preferred the larger ciliate (which was 1/3 of its own body size), suggesting that the longer handling times of the larger prey are rewarding when the large prey is present in high numbers. In terms of total numbers consumed, copepods fed on more small ciliates, but in terms of carbon units both ciliates were selected equally when total prey concentration was low or medium. However, copepods derived more carbon from the larger prey at high and very high prey concentrations (up to 0.7 μgC out of a maximum of 1.1 μgC copepod^?1 h^?1). Habitat complexity influenced the feeding of copepods when it was observed over time. 4. The copepod–ciliate link is well known from the pelagic zone of both marine and freshwater habitats. We have shown its potential importance within the benthos, where it can be influenced by food identity, food quantity and possibly by habitat complexity.     

Acquired phototrophy in Mesodinium and Dinophysis – A review of cellular organization,prey selectivity,nutrient uptake and bioenergetics

Acquired phototrophy, i.e. the use of chloroplasts from ingested prey, can be found among some species of dinoflagellates and ciliates. The best studied examples of this phenomenon in these groups are within the ciliate genus Mesodinium and the dinoflagellate genus Dinophysis, both ecologically important genera with a worldwide distribution. Mesodinium species differ considerably in their carbon metabolism. Some species rely almost exclusively on food uptake, while other species rely mostly on photosynthesis. In Mesodinium with acquired phototrophy, a number of prey organelles in addition to chloroplasts may be retained, and the host ciliate has considerable control over the acquired chloroplasts; Mesodinium rubrum is capable of dividing its acquired chloroplasts and can also photoacclimate. In Dinophysis spp., the contents of ciliate prey are sucked out, but only the chloroplasts are retained from the ingested prey. Some chloroplast house-keeping genes have been found in the nucleus of Dinophysis and some preliminary evidence suggests that Dinophysis may be capable for photoacclimation. Both genera have been claimed to take up inorganic nutrients, including NO₃⁻, indicating that processes beyond photosynthesis have been acquired. M. rubrum seems to depend upon prey species within the Teleaulax/Plagioselmis/Geminigera clade of marine cryptophytes. Up until now, Dinophysis species have only been maintained cultured on M. rubrum as food, but other ciliates may also be ingested. Dinophysis spp. and M. rubrum are obligate mixotrophs, depending upon both prey and light for sustained growth. However, while M. rubrum only needs to ingest 1–2% of its carbon demand per day to attain maximum growth, Dinophysis spp. need to obtain about half of their carbon demand from ingestion for maximum growth. Both Mesodinium and Dinophysis spp. can survive for months in the light without food. The potential role for modeling in exploring the complex balance of phototrophy and phago-heterotrophy, and its ecological implications for the mixotroph and their prey, is discussed.     

Ecological balance between ciliate plankton and its prey candidates,pico- and nanoplankton,in the East China Sea

Standing stocks of ciliate plankton and its prey candidates, both picoplankton and nanoplankton, were investigated in spring in the East China Sea. The former was 1.36 × 10⁵–1.54 × 10⁸ μm³ l⁻¹ in biovolume, and the latter was 5.33 × 10⁶–1.11 × 10⁸ μm³ l⁻¹. The biovolume ratio of ciliate plankton to prey candidates ranged from 1.31 × 10⁻² to 2.00 × 10⁰; it was larger in abundant prey conditions and smaller in sparse preys. Making some plausible assumptions about physiological activity on both organisms, every ratio meet the quantitative restriction that prey production should be equal to or larger than ciliate consumption. However, prey candidates would be so sparsely distributed that ciliate plankton could not capture sufficient prey organisms in its random filter-feeding manner. Even though planktonic ciliates must have some extraordinary mechanisms to capture preys efficiently, this quantitative imbalance might be one of the reasons for decreasing ciliate/prey ratio in sparse prey conditions. Handling editor: K. Martens     

Effects of prey motility and concentration on feeding in Acartia tonsa and Temora longicornis: the importance of feeding modes

Feeding experiments were conducted with the ambush-feeding copepodAcartia tonsa and the feeding-current-generating copepod Temoralongicornis. The copepods were offered a mixed diet of the dinoflagellateHeterocapsa triquetra and the ciliate Balanion comatum of similarcell size. The dinoflagellate was offered at a constant concentrationof 10–15 cells mL^–1, whereas the ciliate was offeredat a variety of concentrations, ranging from 7 to 57 cells mL^–1.Copepods with different feeding modes possess different mechanismsfor prey detection, suggesting that the two copepods would responddifferently to the two prey types. Both copepods had significantlyhigher clearance rates on the highly motile ciliate than onthe less motile dinoflagellate. In encounters between A. tonsaand its prey, we argue that this is due to the higher hydromechanicalsignal generated by the ciliate. The advection feeding copepodT. longicornis fed on the two prey according to their relativeconcentrations; in this case, we suggest that although B. comatumis capable of detecting feeding-current-generating predators,the feeding current velocity generated by T. longicornis isgreater than the escape velocity of this ciliate.     

psbA based molecular analysis of cross-feeding experiments suggests that Dinophysis acuta does not harbour permanent plastids

Toxic marine dinoflagellate species of the genus Dinophysis Ehrenberg are obligate mixotrophs that require feeding on the ciliate Mesodinium rubrum and light to achieve growth. It is now well known that they harbour plastids of cryptophyte origin, particularly of the genus Teleaulax, Plagioselmis or Geminigera group (TPG clade). Nevertheless, whether these plastids are permanent, or periodically acquired from M. rubrum prey, need additional studies in different phototrophic Dinophysis species. The origin of plastids from Dinophysis acuta Ehrenberg, one of the main agents of diarrhetic shellfish poisoning (DSP) outbreaks in Western Europe, was investigated here. Cross feeding-starvation experiments were carried out with cultures of D. acuta using M. rubrum as prey, the latter fed with two cryptophyte species, Teleaulax amphioxeia Hill and Teleaulax gracilis, belonging to the TPG clade in addition to Falcomonas sp. and Hemiselmis sp. The fate of cryptophyte plastids transferred to D. acuta through its ciliate prey was investigated using the plastid psbA gene as a tracer.     

Ultrastructure and Ecology of Perispira ovum (Ciliophora: Litostomatea): An Aerobic, Planktonic Ciliate that Sequesters the Chloroplasts, Mitochondria, and Paramylon of Euglena proxima in a Micro-oxic Habitat

ABSTRACT. High resolution sampling of the stratified water column in a fjord-like ecosystem revealed a green-pigmented planktonic ciliate that was found to be a ravenous predator of Euglena proxima. The vertical distributions of both predator and prey were coincident, and maximum populations occurred across the transition from oxic to anoxic water. This ciliate was identified as Perispira ovum (family Spathidiidae; Order Haptorida). P. ovum was observed by transmission electron microscopy to retain not only the chloroplasts, but also the mitochondria and paramylon reserve of its algal prey. A mechanism of sequestration of algal organelles is demonstrated for the first time. This mechanism includes: recognition, capture, and ingestion of prey; rupture and release of algal cell contents; and enrobing of individual organelles and paramylon by the host vacuolar membrane. The structural integrity, peripheral location, and association with host endoplasmic reticulum suggests the sequestered organelles may be functional within P. ovum. The occurrence and high biomass of this aerobic ciliate in an oxygen-limited environment also suggests that the sequestered chloroplasts are photosynthetically active and may provide additional substrates (such as oxygen) and metabolic capabilities that are crucial for its survival.     

Reproductive success of the rotifer Brachionus calyciflorus feeding on ciliates and flagellates of different trophic modes

SUMMARY 1. The nutritional value of the bacterivorous ciliate Tetrahymena pyriformis and the algivorous ciliate Coleps sp., as well as the heterotrophic flagellate Chilomonas paramecium and the autotrophic flagellate Cryptomonas ovata , were investigated in population growth experiments using the rotifer B. calyciflorus . The two ciliates, both flagellates, which were of similar size, shape and mobility, were each offered as a sole diet and as a supplement to the alga Monoraphidium minutum , known to support reproduction of B. calyciflorus .
2. To further test nutritional differences between the prey organisms, prey selection experiments were conducted in which B. calyciflorus was able to select between the bacterivorous and algivorous ciliate, and between the heterotrophic and autotrophic flagellate.
3. The results demonstrated that both ciliates and the heterotrophic flagellate were not sufficient to support reproduction of B. calyciflorus when offered as a sole diet. They were, however, a good supplement to algal prey (except for the bacterivorous ciliate T. pyriformis ). In the prey selection experiments, B. calyciflorus positively selected for the algivorous Coleps sp. and the autotrophic C. ovata.
4. Overall, ciliates and heterotrophic flagellates may enhance survival of B. calyciflorus , but reproduction of the rotifer is likely to rely on algal prey. Both higher population growth of B. calyciflorus when fed the algivorous Coleps and the autotrophic Cryptomonas, along with their positive selection, give evidence for prey specific differences in nutrition, with algivorous or autotrophic prey species tending to be of higher nutritional value.     

Chemoattraction of a bactivorous ciliate to bacteria surface compounds

The locomotory response to cell surface compounds extracted from two prey species,Vibrio natriegens andVibrio neries, was tested for a bacterivorous ciliate,Pseudochnilembus marinus Thompson 1966. Chemoattraction of the ciliate to the surface compounds stabilized in agarose baits was not equal for the two prey species. Fractionation of the extracts suggested the attractive substance was a high molecular weight compound. The expression of the differential response was dependant on the physiological condition and prior prey species exposure of the ciliate test population. The recognition and response to material normally found on the surface of prey cells supports evidence for the involvement of chemical sensing of gradients of prey particles and dissolved compounds of prey origin in the natural swimming behavior of bacterivorous ciliates. The prey species-specific reactions and influence of ciliate physiological state on chemosensory response suggest ciliate-bacteria interactions may be more complex than preciously assumed.     

Factors affecting preference responses of the freshwater ciliate Uronema nigricans to bacterial prey

ABSTRACT. To enhance our understanding of the factors affecting feeding selectivity of bacterivorous protists in aquatic systems, we examined the preference responses of the freshwater ciliate Uronema nigricans towards three bacterial prey taxa, Pseudomonas luteola, Serratia rubidaea , and Aeromonas hydrophila . Potential factors influencing the predator–prey contact rate included the previous feeding history of the ciliate and physiological state of bacteria. Preference indexes were obtained from multiple-choice mazes in which ciliates moved preferentially towards alternative bacteria or the prey species on which they had been feeding. Uronema nigricans showed differential attraction towards the offered prey types, and these preferences varied as a function of the ciliate feeding history: U. nigricans growing on P. luteola showed lower preference responses towards the offered bacteria than U. nigricans growing on S. rubidaea . The bacteria in stationary phase elicited a higher degree of attraction than bacteria in exponential phase, probably due to a higher concentration of carbohydrates in the former. Therefore, this protist will preferentially swim towards bacteria in stationary growth phase, although the degree of this response will be affected by the recent feeding history of the ciliate.     

Studies on an Astomatous Ciliate From a Fresh-water Limpet, Ferrissia peninsulae

An astomatous holotrichous ciliate inhabiting the excretory tubule of the freshwater gastropod Ferrissia peninsulae is believed to be conspecific with Dogielella renalis Kay, found originally in the renal organ of an unidentified species of another pulmonate genus, Physa. The organization of the ciliary system and the arrangement of the contractile vacuole pores suggest that it is closely related to members of the hymenostomatous genus Tetrahymena, and that it has evolved from a ciliate of this general type through loss of the cytostome and cytostomal membranelles.
Because it is not possible at present to state with certainty that this ciliate is congeneric with D. sphaerii, the genotype of the genus Dogielella Poljanskij, a new genus, Curimostoma, is established for it. Curimostoma is referred provisionally to the family Tetrahymenidae.     

Short‐term temperature change may impact freshwater carbon flux: a microbial perspective

Small freshwater bodies are abundant and economically and ecologically important on a global scale. Within these, protozoa play an important role in structuring planktonic food webs and sequestering CO₂. We hypothesized that short‐term (～20 days) fluctuations, of 2–10 °C, will significantly alter carbon flux associated with predator–prey interactions within the microbial planktonic food web. We examined the model ciliate, Urotricha farcta, which is abundant and common; it was fed the autotrophic flagellate Cryptomonas sp., which is also common. Laboratory experiments were conducted over relevant ranges: 8–24 °C; 0–2 × 10⁵ prey mL^?1. Mechanistic‐phenomenological multiple regressions were developed and fit to the data to obtain relationships for (1) growth rate and volume changes of the flagellate vs. temperature and (2) growth rates, grazing, and cell volume change of the ciliate vs. temperature and prey concentration. Responses revealed interaction between temperature and prey levels on all ciliate parameters, indicating it is inappropriate to apply simple temperature corrections (e.g. Q₁₀) to such functions. The potential impact of such temperature changes on carbon flux was illustrated using a simple ciliate–flagellate predator–prey model, with and without the top grazer, Daphnia, added. The model indicated that predator–prey pulses occurred over 20 days, with the ciliate controlling the prey population. For ciliates and prey, carbon production peaked at 20 °C and rapidly decreased above and below this maximum; differences between minimum and maximum were approximately fourfold, for both prey and ciliate, with low levels at 25–30 °C and 10–15 °C. Including literature data to parameterize, the influence of the grazer Daphnia did not alter the prediction that the ciliate may control short‐term flagellate pulses and temperature will influence these in a nonintuitive fashion.     

Molecular characterization and revised systematics of Microdiaphanosoma arcuatum (Ciliophora, Colpodea)

Microdiaphanosoma arcuatum Wenzel, 1953 is a world-wide distributed ciliate, recorded mainly in soil samples, which we have also identified in ground water samples from South Africa. This ciliate has been frequently overlooked or not determined due to its small size, ～12 μm. The genus Microdiaphanosoma is nowadays included in the class Colpodea, order Bryometopida, family Kreyellidae. The first complete small subunit (SSU) rDNA gene sequence of this ciliate was obtained from a South African isolate. Phylogenetic analysis including available SSU rDNA sequences from another Colpodea species in the GenBank strongly supported the position of M. arcuatum within the order Cyrtolophosidida instead of the order Bryometopida. The analysis also suggested a sister relationship between this species and species from the family Cyrtolophosididae.     

Isolation of the Lembadion-factor,A morphogenetically active signal,that induces Euplotes cells to change from their ovoid form into a larger lateral winged morph

A morphogenetically active substance released by the predatory ciliate Lem-badion bullinum is recognized by ciliates of the genus Euplotes, which are potential prey organisms of Lembadion. The substance (L-factor) induces cells of the genus Euplotes to become less compact, which reduces their likelihood of becoming engulfed. Under the influence of this Lembadion- derived signal, E. octocarinatus develops extended wings and dorsal and ventral ridges and transforms within a few hours from its typical ovoid morph into an enlarged circular morph. This takes place without cell division. We have isolated the L-factor and report that it is a protein with a mass of 31,500 Da. The factor has been purified to chromatographic and electrophoretic homogeneity and was found to be active at concentrations as low as 10^?12 mol/L. © 1992 Wiley-Liss, Inc.     

Encystment-inducing factors in the ciliate Euplotes elegans

Although starvation is considered one of the most important induces of ciliate encystment, its nature has been unclear. Euplotes is a well-known ciliate genus, but the relationship in Euplotes between encystment and food has not been reported. The encystment of Euplotes elegans is facilitated when it is transferred to Chalkley's solution without bacteria as food. A higher ciliate density also facilitates encystment. Thus, starvation and ciliate density needed to be examined. Ciliates were inoculated into 3 treatments: Chalkley's solution with formaldehyde-fixed bacteria as nutritive particles (FFB group), with polystyrene latex particles as non-nutritive particles (PLP group), and without particles (control group). Cysts appeared fastest and ciliate numbers increased in the FFB group. Although the encystment kinetics of the PLP group was similar to that of the control group, the encystment rate of the PLP group was lower than that of the control group in the earliest phase. This suggests that the ciliates were temporarily deceived into feeding on PLP, because they had food vacuoles containing PLP during the earliest phase of incubation. A cell-free old culture solution from a stationary phase, which probably contained excreted substances from high-density ciliates, also facilitated encystment.     

Preferential Plastid Retention by the Acquired Phototroph Mesodinium chamaeleon

The ciliate genus Mesodinium contains species that rely to varying degrees on photosynthetic machinery stolen from cryptophyte algal prey. Prey specificity appears to scales inversely with this reliance: The predominantly phototrophic M. major/rubrum species complex exhibits high prey specificity, while the heterotrophic lineages M. pulex and pupula are generalists. Here, we test the hypothesis that the recently described mixotroph M. chamaeleon, which is phylogenetically intermediate between M. major/rubrum and M. pulex/pupula, exhibits intermediate prey preferences. Using a series of feeding and starvation experiments, we demonstrate that M. chamaeleon grazes and retains plastids at rates which often exceed those observed in M. rubrum, and retains plastids from at least five genera of cryptophyte algae. Despite this relative generality, M. chamaeleon exhibits distinct prey preferences, with higher plastid retention, mixotrophic growth rates and efficiencies, and starvation tolerance when offered Storeatula major, a cryptophyte that M. rubrum does not appear to ingest. These results suggest that niche partitioning between the two acquired phototrophs may be mediated by prey identity. M. chamaeleon appears to represent an intermediate step in the transition to strict reliance on acquired phototrophy, indicating that prey specificity may evolve alongside degree of phototrophy.     

Detecting In Situ Copepod Diet Diversity Using Molecular Technique: Development of a Copepod/Symbiotic Ciliate-Excluding Eukaryote-Inclusive PCR Protocol

Knowledge of in situ copepod diet diversity is crucial for accurately describing pelagic food web structure but is challenging to achieve due to lack of an easily applicable methodology. To enable analysis with whole copepod-derived DNAs, we developed a copepod-excluding 18S rDNA-based PCR protocol. Although it is effective in depressing amplification of copepod 18S rDNA, its applicability to detect diverse eukaryotes in both mono- and mixed-species has not been demonstrated. Besides, the protocol suffers from the problem that sequences from symbiotic ciliates are overrepresented in the retrieved 18S rDNA libraries. In this study, we designed a blocking primer to make a combined primer set (copepod/symbiotic ciliate-excluding eukaryote-common: CEEC) to depress PCR amplification of symbiotic ciliate sequences while maximizing the range of eukaryotes amplified. We firstly examined the specificity and efficacy of CEEC by PCR-amplifying DNAs from 16 copepod species, 37 representative organisms that are potential prey of copepods and a natural microplankton sample, and then evaluated the efficiency in reconstructing diet composition by detecting the food of both lab-reared and field-collected copepods. Our results showed that the CEEC primer set can successfully amplify 18S rDNA from a wide range of isolated species and mixed-species samples while depressing amplification of that from copepod and targeted symbiotic ciliate, indicating the universality of CEEC in specifically detecting prey of copepods. All the predetermined food offered to copepods in the laboratory were successfully retrieved, suggesting that the CEEC-based protocol can accurately reconstruct the diets of copepods without interference of copepods and their associated ciliates present in the DNA samples. Our initial application to analyzing the food composition of field-collected copepods uncovered diverse prey species, including those currently known, and those that are unsuspected, as copepod prey. While testing is required, this protocol provides a useful strategy for depicting in situ dietary composition of copepods.     

<Emphasis Type="Italic">Notohymena saprai</Emphasis> sp. nov,a new oxytrichid ciliate (Protozoa,Ciliophora) from the Valley of Flowers,a Himalayan bioreserve region; description and morphogenesis of the new species

A new oxytrichid ciliate Notohymena saprai sp. nov was isolated from the Valley of Flowers, an isolated bioreserve in the upper Himalayas. The ciliate was found in the soil samples collected from the peripheral areas of the flowering region of the valley which is covered with permafrost for nearly eight months in a year. Cells were excysted from the soil samples by the non-flooded petridish method. Species identification was performed by observations on live and silver-impregnated cells. Notohymena saprai sp. nov is highly flexible, measures 152 × 49 μm and shows abundant presence of dark green sub-pellicular granules. The species is distinct by virtue of its new combination of morphometric and developmental characters. Prominent distinguishing features of the new species are its relative large size and presence of four macronuclei (other species of this genus have two macronuclei). The study also reports morphogenetic peculiarities which separate it from the other known species of the genus.