Non-lethal presence of predators modifies morphology and movement rates in <Emphasis Type="Italic">Euplotes</Emphasis>

Many species are able to modify aspects of their behaviour and morphology in the presence of predators. The aim of this study was to investigate the relationship between the expression of morphological and behavioural defences according to the framework proposed by DeWitt et al (1999). Experiments were carried out using hypotrich ciliates of the genus Euplotes as prey and turbellarians of the genus Stenostomum as predators. The smaller species Euplotes octocarinatus showed a greater proportional increase in width, a reduction in foraging movement rates and an increase in maximum movement rates following exposure to predator cues. The larger Euplotes aediculatus induced lesser changes in width, similar reductions in movement during foraging and no change in maximum speed following predator exposure. These results provide evidence of a cospecialised relationship between morphological and behavioural defences. Despite substantial differences in the absence of predators, movement rates and lateral body width were similar in both species following predator exposure. The observed changes may be considered adaptive, gape limited flatworm predators are unable to ingest large Euplotes and a reduction in movement rates during foraging reduces predator encounter rates, while an increase in maximal movement rates increases chances of predator evasion. Handling editor: S. I. Dodson     

Predation risk of typical ovoid and ‘winged’ morphs of Euplotes (Protozoa,Ciliophora)

Freshwater species of the genus Euplotes (Protozoa, Ciliophora) change their morphology in the presence of some of their predators. The ciliates develop extended lateral wings as well as dorsal and ventral projections which make engulfment by predators more difficult. In a series of laboratory experiments ingestion rates of four protozoan predators, the ciliates Lembadion bullinum, Dileptus anser, Stylonychia mytilus and Urostyla grandis, and one metazoan predator, the turbellarian Stenostomum sphagnetorum, on three species of Euplotes (E. octocarinatus, E. patella and E. aediculatus) were determined. It was calculated that the probability of rejection by a predator changed from 1:1 for ovoid morphs of Euplotes to about 2:1–20:1 for winged morphs of Euplotes, dependent on the prey and predator species that were combined. The nutritional condition of the prey also had some influence. In mixed-species cultures of prey and predators, transformed cells of E. octocarinatus survived for several months.     

Effects of food availability on predator-induced morphological defence in the ciliate Euplotes octocarinatus (Protista)

The effect of a prey's food resources on predator-induced morphological transformation was studied in two ciliate species: Euplotes octocarinatus (prey) and Stylonychia mytilus (predator). The ability to produce defence in Euplotes was much reduced by prolonged starvation. The extent of prey morphological transformation and therefore the effectiveness of the defence was inversely related to the length of time without food. The results suggest that the defence involves an energetic cost which may be a significant part of the whole cell budget, at least when food is in short supply. Not only the morphological transformation but also the maintenance of the anti-predator phenotype were energetically costly for Euplotes, the cost being proportional to the defence level. The morphological transformation was affected by the kind of food (algae) provided to the prey. Ciliates fed Chlorogonium elongatum attained their maximum width sooner than those fed Chlamydomonas. Thus, both the quantity and the quality of the food available may significantly affect the magnitude of response and therefore the potential success of an induced defence.     

Induction of defensive morphological changes in ciliates

Freshwater ciliates of the genusEuplotes change their morphology in response to the presence of predators. The morphological transformations limit the ability of the predators to ingest the ciliates. Induction of defensive morphology by the predatorsStenostomum sphagnetorum (Turbellaria),Lembadion bullinum (Ciliata),L. magnum, andAmoeba proteus (Rhizopoda) was studied inEuplotes aediculatus andE. octocarinatus. The results suggest the possibility of natural occurrence of predator-induced defensive morphology inEuplotes. A density of 1 predator ml⁻¹ was sufficient to induce significant changes in the morphology ofEuplotes. L. magnum was found at natural population densities of 5 individuals ml⁻¹. Transformations can take place within 2–4 h. Morphological changes are induced by signal substances released from the predators; direct contact between prey and predators is not necessary. The extent of transformation depends on the concentration of the signal substance. The size frequency distribution of the populations only had one peak that was related to predator density. All individuals of a population ofEuplotes changed their morphology according to the predator abundance. This may reduce energy costs for the prey by prevention of unnecessary morphological changes.Amoeba proteus induces morphological changes inE. octocarinatus, but not inE. aediculatus.     

Effect of Algal Food on Animal Prey Consumption Rates in the Omnivorous Copepod,Mesocyclops thermocyclopoides

We measured the food consumption rates in the omnivorous copepod Mesocyclops thermocyclopoides on different animal prey types in the presence of, and in the absence of one of the algal food types, the small, nonmotile Chlorella, or the large, motile Chlorogonium. Animal prey tested included different zooplankton species covering a size range of 88 to 1446 μm. The number of animal prey consumed was inversely proportional, but the total weight consumed was directly proportional, to the body size and dry weight of the prey item. There was a significant reduction in animal prey consumption in the presence of algae, being higher with cladoceran prey than with ciliates and rotifers, and in the presence of Chlorogonium than in the presence of Chlorella. Cannibalism in M. thermocyclopoides was low when algal food was available.     

Intranuclear Parasitism of the Ciliate Euplotes by a Trypanosomatid Flagellate

A trypanosomatid flagellate, Leptomonas sp., develops and multiplies in the macronucleus (only) of natural and laboratory-reared populations of the ciliate Euplotes. Up to 90% of the natural populations of Euplotes in our test pond had such nuclear infections. Laboratory infections were transmitted to this ciliate by feeding it liberated parasites. Paramecium resisted infections. All laboratory-induced infections were lethal to Euplotes, while control clones of the uninfected ciliates remained viable. This leptomonad, unlike Leptomonas karyophilus (found in Paramecium), shows no leishmanial forms in its several ciliate hosts and shows a varied pattern of locomotion.     

The Behavior and Fine Structure of the Dorsal Bristles of Euplotes minuta,E. aediculatus,and Stylonychia mytilus (Ciliata,Hypotrichida)1

ABSTRACT. Studies of the bristle (dorsal) cilia of Euplotes minuta. E. aediculatus, and Stylonychia mytilus by light and electron microscopy indicate that these cilia do not beat metachronously in any of the species. The bristle cilia in Stylonychia may beat actively, but those in Euplotes stand erect or are bent in different directions with the flow of water. The duration and degree of bending appear correlated with the duration and velocity of the water current. The fine structure of the bristle complex is similar in both Euplotes species and like other reports of Euplotes in the literature. The complex consists of paired kinetosomes, the anterior bearing a short cilium containing four to six rows of fibrous balls (lasiosomes) oriented along the anterior surface of the axoneme, the posterior lacking a cilium but with a small cap. Microtubular ribbons are associated with the paired kinetosomes, and a collar with a pronounced alveolar ring underneath the pellicular membrane tightly surrounds the cilium at the opening of the bristle pit. The bristle complex in S. mytilus differs from that of Euplotes and other hypotrichs in that it has a single kinetosome in interphase cells and, attached to the kinetosome, a prominent fibrous structure (parakinetosomal body). Microtubules are attached to the parakinetosomal body. As in Euplotes, the bristle unit is surrounded by mucocyst-like organelles (ampules). Observations of behavior and fine structure suggest that the dorsal bristles may be sensory, perhaps responding to stimuli from water currents, although other functions are possible, too.     

Optimal foraging: the difficulty of exploiting different feeding strategies simultaneously

Summary The foraging efficiency of a visually feeding fish, perch (Perca fluviatilis) was studied on two prey species (Daphnia magna and Chaoborus obscuripus) presented either separately or combined. It is shown that when both prey species are present, the foraging efficiency of the predator is reduced. This is due to the predator's inability to simultaneously cope with prey species with different anti-predatory behaviour. In the mixed-meal experiment the predator captured both prey species in equal proportions in disagreement with optimal foraging models assuming that handling time and encounter rate for a prey species are independent of other prey species. The results are, however, in agreement with optimal foraging models assuming that handling time and encounter rate are influenced by short time learning.     

Predatory behavior of Cupelopagis vorax (Rotifera; Collothecacea; Atrochidae) on protozoan prey

By rotating on a short, flexible, pedal stalk, Cupelopagis vorax captures prey that traverse the substratum to which this sessile rotifer attaches. Microvideographic analysis (including slow motion and freeze-frame) permitted us to examine some of the details of Cupelopagis foraging behavior. When undisturbed, Cupelopagis usually faces forward in a resting or neutral position (NP) with its unciliated infundibulum (corona) directed parallel to the surface of the substratum. However, vibrations produced by artificial means (fine pins) or small prey (protists) evoke unique behaviors in Cupelopagis. Our analysis of Cupelopagis foraging on two protozoan prey (Paramecium bursaria and a small, unidentified flagellate, SUF) indicates that this predator possesses a 360 ° encounter field (EF) biased towards the NP Size of the EF appears to be a function of both predator and prey size, but it extends at least 650 µm, as measured from the point of attachment of the predator's pedal stalk to the substratum. When a prey comes close to Cupelopagis, this predator can lean toward the organism, stretching forward on its pedal stalk and extending its corona over the prey in a swift motion (< 0.5 s). Probability of capture after attack was a function of prey type (61.6% for P. bursaria and 41.5% for the SUF). Analysis of prey capture by Cupelopagis indicates that this predator has a handling time ranging from a few seconds to several minutes: 24.6 ± 16.8 s for P. bursaria (n= 274) and 34.6 ± 25.4 s for the SUF (n=111). Occasionally Cupelopagis sweeps part of the EF by retracting its corona, turning to the right or left (mean angle subtended 63 ° ± 42 °), unfolding the corona, and slowly returning to the original resting position. This behavior, termed surveillance, occurs in the presence or absence of prey. While not unique in its ability to detect water movements, Cupelopagis is the only rotifer known to exhibit specific behaviors to vibrations produced by potential prey.     

The functional responses of two benthic algivorous ciliated protozoa with differing feeding strategies

Surface-associated algivorous ciliated protozoa are common in the benthos of streams, but little is known about the feeding ecology of these organisms. We compared the functional responses of two algivorous ciliated protozoa, Oxytricha fallax (a filter feeder) and Trithigmostoma cucullulus (an encounter feeder). The ciliates were fed ¹⁴C-labeled Navicula cryptocephala in laboratory feeding experiments to determine their potential to consume significant amounts of algal prey. Logistic regression, and plots of the proportion of N. cryptocephala ingested vs. the total number offered, indicated functional responses of a typical rectangular hyperbolic (type II) form for both ciliates. Ingestion rates were estimated from regressions of the number of ¹⁴C-labeled N. cryptocephala cells ingested per ciliate vs. time. Maximum feeding rates and half-saturation concentrations were estimated by fitting the observed ingestion rates and experimental algal densities to a function of the Michaelis-Menten enzyme kinetics form using nonlinear regression. For O. fallax, the maximum feeding rate was estimated to be 1.07 N. cryptocephala cells per minute, and the half-saturation concentration was 3.9 × 102 N. cryptocephala per square centimeter. For T. cucullulus the maximum feeding rate was estimated to be 0.2 N. cryptocephala per minute, and the half-saturation concentration was 5.4 × 10³ N. cryptocephala per square centimeter. The data were also fitted using only the number of cells ingested at 60 and 120 min, by converting the endpoint consumption to rates. For O. fallax, the estimated maximum feeding rates were 1.3 and 1.0 N. cryptocephala per minute for 60 and 120 min, respectively, and estimated half-saturation concentrations were 5.1 × 10² and 3.5 × 10² N. cryptocephala per square centimeter. For T. cucullulus, estimated maximum feeding rates were 0.6 and 0.4 N. cryptocephala per minute for 60 and 120 min, respectively, and estimated half-saturation concentrations were 1.5 × 10⁴ and 1.1 × 104 N. cryptocephala per square centimeter. These results suggest that kinetic methods for estimating ingestion rates are more accurate than endpoint determinations. Based on field observations of periphyton densities, these ciliates potentially are consuming 4.8% of the total available standing crop of diatom biomass per day and this could represent up to 16% of total available daily primary production.     

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.     

Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod

Omnivorous arthropods make dietary choices according to the environment in which they forage, mainly availability/quality of plant and/or prey resources. Such decisions and their subsequent impacts on life‐history traits may be affected by the availability of nutrients and water to plants, that is, through bottom‐up forces. By setting up arenas for feeding behavior observation as well as glasshouse cages for plant preference assessment, we studied effects of the presence of prey (Lepidoptera eggs) and nitrogen/water availability to host tomato plants on the foraging behavior and life‐history traits in the omnivorous predator Macrolophus pygmaeus (Heteroptera: Miridae). In the absence of prey, the predator fed equally on the plants treated with various levels of nitrogen and water. In the presence of prey, however, the feeding rate on plants decreased when the plant received low water input. The feeding rate on prey was positively correlated with feeding rate on plants; that is, prey feeding increased with plant feeding when the plants received high water input. Moreover, plants receiving high water input attracted more M. pygmaeus adults compared with those receiving low water input. For M. pygmaeus fitness, the presence of prey enhanced its fertility and longevity, but the longevity decreased when plants received low compared with high water input. In conclusion, the omnivorous predator may be obliged to feed on plants to obtain water, and plant water status may be a limiting factor for the foraging behavior and fitness of the omnivorous predator.     

Ingestion and assimilation by marine protists fed on bacteria labeled with radioactive thymidine and leucine estimated without separating predator and prey

A procedure has been developed for preparing living bacteria, quantitatively labeled with ³H-thymidine and ¹⁴C-leucine, for short-term grazing experiments. The negligible rate of accumulation in protozoan macromolecules of moieties of bacterial macromolecules labeled with ³H compared with moieties labeled with ¹⁴C permits estimation of the consumption, digestion, and assimilation of prey biomass in protists without separating them from bacteria. The principles of this method are described, and the results of its application in examples of grazing by the ciliates Euplotes and Uronema and the flagellate Pteridomonas on the bacterium Vibrio are outlined. Correspondence to: M.A. Sleigh     

Effects of grazers' species identity on cyanobacteria in bitrophic and tritrophic food webs

Using laboratory microcosms, we studied direct and indirect interactions among different components of bi- and tritrophic communities. Filamentous cyanobacteria ( Phormidium sp.) and autotrophic flagellates ( Chlorogonium elongatum ) were primary producers. The second trophic level was represented by ciliates Furgasonia blochmanni and Pseudomicrothorax dubius grazing on the filamentous cyanobacteria and two filter feeders, Euplotes octocarinatus and Stylonychia pustulata , feeding on the autotrophic flagellates. An oligochaete, Chaetogaster sp., was used as the top predator. An experiment was carried out for all combinations of two factors: (1) the identity of the cyanobacteria consumer ( Furgasonia or Pseudomicrothorax ) and (2) the presence or absence of the top predator. Significant effects of the treatments on both the abundance of cyanobacteria and filter feeding ciliates and predator-induced defense in Phormidium and Euplotes were observed in a 36-day experiment. The experiment showed that the substitution of one species ( Furgasonia ) for another ( Pseudomicrothorax ) seemingly playing the same ecological role may lead to significant changes in the whole community.     

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.     

Characterization of the pheromone gene family of an Antarctic and Arctic protozoan ciliate, Euplotes nobilii

Allelic genes encoding water-borne signal proteins (pheromones) were amplified and sequenced from the somatic (macronuclear) sub-chromosomic genome of Antarctic and Arctic strains of the marine ciliate, Euplotes nobilii. Their open reading frames appeared to be specific for polypeptide sequences of 83 to 94 amino acids identifiable with cytoplasmic pheromone precursors (pre-pro-pheromones), requiring two proteolytic steps to remove the pre- and pro-segments and secrete the mature pheromones. Differently from most of the macronuclear genes that have so far been characterized from Euplotes and other hypotrich ciliates, the 5′ and 3′ non-coding regions of all the seven E. nobilii pheromone genes are much longer than the coding regions (621 to 700 versus 214 to 285 nucleotides), and the 5′ regions in particular show nearly identical sequences across the whole set of pheromone genes. These structural peculiarities of the non-coding regions are likely due to the presence of intron sequences and provide presumptive evidence that they are site of basic, conserved activities in the mechanism that regulates the expression of the E. nobilii pheromone genes.     

Adaptation of inducible defense in Euplotes daidaleos (Ciliophora) to predation risks by various predators

The extent of induced morphological defense in Euplotes daidaleos correlates to this ciliate's predation risk from the defense-inducing predator species. Euplotes daidaleos responded by morphological transformation only to organisms that are able to feed on typically formed Euplotes cells (63 ± 5 m cell width in E. daidaleos). Three of those potential predator species caused defensive changes to various degrees (Student's t-test, P < 0.1 to P < 0.0001): Lembadion bullinum (Ciliata) induced 82 ± 6 m cell width in E. daidaleos; Chaetogaster diastrophus (Oligochaeta) induced 85 = 6 m width; and Stenostomum sphagnetorum (Turbellaria) induced 89 ± 8 m width (at a density of 10 predators per milliliter, respectively). At higher predator densities (50 or 100 organisms per milliliter), Euplotes developed a correspondingly larger width (to a maximum of 103 ± 10 m in the presence of S. sphagnetorum). Euplotes did not respond to organisms (e.g., Blepharisma japonicum, Colpidium campylum, Didinium nasutum, Paramecium caudatum, Spirostomum ambiguum, Stentor coeruleus) that cannot feed on this ciliate species. Daphnia longispina and Bursaria truncatella predators, which can feed on large prey of 125, or 200 m in diameter, respectively, also had no effect on the morphology of Euplotes. The extent of defense in Euplotes that was induced by 10 predators per milliliter during 24 h decreased the predation risk from those predators to 67% in the presence of S. sphagnetorum, to 50% with L. bullinum, and to 15% with C. diastrophus, compared to the typical form of Euplotes. In a natural population, the defensive form of E. daidaleos was found with average cell widths of 88 ± 8 m. The results indicate that predator-induced defense in natural Euplotes populations is beneficial to this prey and that it is adapted to the predation abilities of Euplotes predators, whereby energetical costs related to defensive changes may be saved.     

Behavioural and morphological changes in ciliates induced by the predator Amoeba proteus

The predator Amoeba proteus induced behavioural and morphological changes in ciliates of the genus Euplotes. The frequency of avoidance behaviour in E. octocarinatus increased from 16±5% to 84±5% (SD) after 14 h of coexistence with the predator. The ciliate's width increased from 59±3 μm to 77±4 μm (SDM) within 48 h. Similar behavioural, but not morphological, change was induced in E. daidaleos, but neither morphological nor behavioural responses occurred in E. aediculatus. E. octocarinatus and E. daidaleos populations survived in the presence of A. proteus, whereas E. aediculatus populations became extinct by predation. Induced behavioural response seemed to be the reason for the low predation risk of E. octocarinatus and E. daidaleos. The results suggest that Euplotes ciliates have evolved specific defence mechanisms to various predators. Defensive changes are induced by a chemical substance released from A. proteus. This “kairomone” has a molecular weight between 5000 and 10000 Da. Proteolytic digestion of its activity indicated that the avoidance-inducing substance is a peptide. After the turbellarian Stenostomum sphagnetorum had induced a defensive morphology in E. octocarinatus or E. aediculatus, neither of these ciliates immediately avoided Amoeba proteus. Thus, Euplotes ciliates with a defensive morphology do not have behavioural defences in reaction to all predators.     

A study of feeding in predacious ciliates using prey ciliates labeled with fluorescent microspheres

Feeding in predacious estuarine ciliates was investigated ina series of laboratory experiments using a new method of preylabeling which facilitates microscopic indentification of ingestedprey items. Ingestion rates of Mesodinium pulex, Euplotes vannusand E.woodruffi were estimated using the appearance, insidethe predator, of bacteriovorous ciliates (Metanophrys sp., Cyclidiumsp.and Pleuronema sp ) labeled with fluorescent microspheres. Preyremain motile and have presumably unaltered surface characteristics.Ingestion rates of log-growth phase predators increased withprey density. Mesodinium pulex ingested 0 15–0.32 cellsh^–1 over a prey concentration of 60–2300 ml^–1.Maximum ingestion rates of E. woodruffi and E. vannus were 4.5and 3.4 cells h^–1 respectively, estimated at prey abundancesof 75 and 172 cells ml^–1 respectively. Comparisons offeeding rates on prey of different sizes, and the effects ofstarvation, indicated that ingestion is likely limited by differentfactors in ‘raptorial’ (M pulex) and ‘filterfeeding’ (Euplotes spp.) predators.     

Effects of satiation on feeding and swimming behaviour of planktivores

Hunger affects the feeding and swimming behaviour in fish. After 36 h of food deprivation, the feeding and swimming behaviour of Pseudorasbora parva (Cyprinidae) was studied under different prey densities (0.5, 1, 2, 5, 10 and 25 of Daphnia pulex per liter). The initial feeding rates showed marked variations in relation to prey availability. Under high prey densities, the initial feeding rate of fish was higher and subsequently decreased faster, when compared to those feeding under low prey densities. At higher prey densities, two factors were involved: that of higher prey encounter rates and also the attainment of food satiation at a faster rate. Across all prey densities, the feeding rates of fish reached a plateau after satiation. The swimming speed of fish was found to be negatively related to the prey density and a significant change in swimming speed was noted as being directly related to the level of satiation. It was found that the increasing satiation level greatly influenced the handling time and reactive volume of predator, which finally caused reduced feeding rates.