A tale of the ciliate tail: investigation into the adaptive significance of this sub-cellular structure

Ciliates can form an important link between the microbial loop and higher trophic levels primarily through consumption by copepods. This high predation pressure has resulted in a number of ciliate species developing rapid escape swimming behaviour. Several species of these escaping ciliates also possess a long contractile tail for which the functionality remains unresolved. We use high-speed video, specialized optics and novel fluid visualization tools to evaluate the role of this contractile appendage in two free-swimming ciliates, Pseudotontonia sp. and Tontonia sp., and compare the performance to escape swimming behaviour of a non-tailed species, Strobilidium sp. Here, we show that ‘tailed’ species respond to hydrodynamic disturbances with extremely short response latencies (less than or equal to 0.89 ms) by rapidly contracting the tail which carries the cell body 2–4 cell diameters within a few milliseconds. This provides an advantage over non-tailed species during the critical first 10–30 ms of an escape. Two small, short-lived vortex rings are created during contraction of the tail. The flow imposed by the ciliate jumping can be described as two well-separated impulsive Stokeslets and the overall flow attenuates spatially as r⁻³. The high initial velocities and spatio-temporal arrangement of vortices created by tail contractions appear to provide a means for rapid escape as well as hydrodynamic ‘camouflage’ against fast striking, mechanoreceptive predators such as copepods.     

Danger of zooplankton feeding: the fluid signal generated by ambush-feeding copepods

Zooplankton feed in any of three ways: they generate a feeding current while hovering, cruise through the water or are ambush feeders. Each mode generates different hydrodynamic disturbances and hence exposes the grazers differently to mechanosensory predators. Ambush feeders sink slowly and therefore perform occasional upward repositioning jumps. We quantified the fluid disturbance generated by repositioning jumps in a millimetre-sized copepod (Re ∼ 40). The kick of the swimming legs generates a viscous vortex ring in the wake; another ring of similar intensity but opposite rotation is formed around the decelerating copepod. A simple analytical model, that of an impulsive point force, properly describes the observed flow field as a function of the momentum of the copepod, including the translation of the vortex and its spatial extension and temporal decay. We show that the time-averaged fluid signal and the consequent predation risk is much less for an ambush-feeding than a cruising or hovering copepod for small individuals, while the reverse is true for individuals larger than about 1 mm. This makes inefficient ambush feeding feasible in small copepods, and is consistent with the observation that ambush-feeding copepods in the ocean are all small, while larger species invariably use hovering or cruising feeding strategies.     

Hydrodynamic interaction between two copepods: a numerical study

Numerical simulations were carried out to compute the flow fieldaround two tethered, stationary or swimming model-copepods withvaried separation distances between them and for different relativebody positions and orientations. Based on each simulated flowfield, the power expended by each copepod in generating theflow field and volumetric flux through the capture area of eachcopepod were calculated. The geometry of the flow field aroundeach copepod was visualized by tracking fluid particles to constructstream tubes. The hydrodynamic force on each copepod was calculated.Also, velocity magnitudes and deformation rates were calculatedalong a line just above the antennules of each copepod. Allthe results were compared to the counterpart results for a solitarycopepod (stationary or swimming) to evaluate the hydrodynamicinteraction between the two copepods. The calculations of thepower and volumetric flux show that no energetic benefits areavailable for two copepods in close proximity. The results ofthe stream tube and force calculations show that when two copepodsare in close proximity, the hydrodynamic interaction betweenthem distorts the geometry of the flow field around each copepodand changes the hydrodynamic force on each copepod. Two beneficialroles of the hydrodynamic interactions are suggested for copepodswarms: (1) to maintain the integrity of the swarms and (2)to separate the swarming members with large nearest neighbourdistances (usually more than five body lengths). To preventstrong hydrodynamic interactions, copepods in swarms have toavoid positions of strong interactions, such as those directlyabove or below their neighbours. The results of the velocitymagnitudes and deformation rates demonstrate that the hydrodynamicinteraction between two copepods generates the hydrodynamicsignals detectable by the setae on each copepod's antennules.Based on the threshold of Yen et al. (1992), the results showthat the detection distance between two copepods of comparablesize is about two to five body lengths. Copepods may employa simple form of pattern recognition to detect the distance,speed and direction of an approaching copepod of comparablesize.     

Dispersal Patterns,Active Behaviour,and Flow Environment during Early Life History of Coastal Cold Water Fishes

During the pelagic larval phase, fish dispersal may be influenced passively by surface currents or actively determined by swimming behaviour. In situ observations of larval swimming are few given the constraints of field sampling. Active behaviour is therefore often inferred from spatial patterns in the field, laboratory studies, or hydrodynamic theory, but rarely are these approaches considered in concert. Ichthyoplankton survey data collected during 2004 and 2006 from coastal Newfoundland show that changes in spatial heterogeneity for multiple species do not conform to predictions based on passive transport. We evaluated the interaction of individual larvae with their environment by calculating Reynolds number as a function of ontogeny. Typically, larvae hatch into a viscous environment in which swimming is inefficient, and later grow into more efficient intermediate and inertial swimming environments. Swimming is therefore closely related to length, not only because of swimming capacity but also in how larvae experience viscosity. Six of eight species sampled demonstrated consistent changes in spatial patchiness and concomitant increases in spatial heterogeneity as they transitioned into more favourable hydrodynamic swimming environments, suggesting an active behavioural element to dispersal. We propose the tandem assessment of spatial heterogeneity and hydrodynamic environment as a potential approach to understand and predict the onset of ecologically significant swimming behaviour of larval fishes in the field.     

Hang on or run? Copepod mating versus predation risk in contrasting environments

Mating durations of copepods were found to differ significantly between fishless high-altitude waters and lowland lakes containing fish. In lowland species the whole mating process was completed within a few minutes, but it averaged over an hour in high-altitude species. Alpine copepods showed a prolonged post-copulatory association between mates, during which the male clasped the female for an extended period after spermatophore transfer, while in lowland species males abandoned their partner immediately after copulation. Prolonged associations also occurred after transfer of spermatophores to heterospecific females with shorter conspecific mating duration, suggesting that male interests largely dictate the time spent in tandem. The differences observed may be adaptations to environments with different predation pressure, as pairs in tandem are more conspicuous and less reactive than single animals. We argue that differences in mating behavior and mating duration evolved under sexual versus natural selection, reflecting trade-offs between enhancement of fertilization success and reduction of vulnerability to visual predation. In fishless mountain lakes with high intrasexual competition, guarding males can reduce the risk of spermatophore displacement or the risk that the female will accept sperm from rival males without increased risk of being eaten, thereby maximizing paternity. Populations from fishless alpine lakes further differed from lowland species by exhibiting higher female/male size dimorphism and more intense pigmentation. While these traits vary between populations according to predation pressure, mating duration appears to be more species-specific.     

Copepod flow modes and modulation: a modelling study of the water currents produced by an unsteadily swimming copepod

Video observation has shown that feeding-current-producing calanoid copepods modulate their feeding currents by displaying a sequence of different swimming behaviours during a time period of up to tens of seconds. In order to understand the feeding-current modulation process, we numerically modelled the steady feeding currents for different modes of observed copepod motion behaviours (i.e. free sinking, partial sinking, hovering, vertical swimming upward and horizontal swimming backward or forward). Based on observational data, we also reproduced numerically a modulated feeding current associated with an unsteadily swimming copepod. We found that: (i) by changing its propulsive force, a copepod can switch between different swimming behaviours, leading to completely different flow-field patterns in self-generated surrounding flow; (ii) by exerting a time-varying propulsive force, a copepod can modulate temporally the basic flow modes to create an unsteady feeding current which manipulates precisely the trajectories of entrained food particles over a long time period; (iii) the modulation process may be energetically more efficient than exerting a constant propulsive force onto water to create a constant feeding current of a wider entrainment range. A probable reason is that the modulated unsteady flow entrains those water parcels containing food particles and leaves behind those without valuable food in them.     

Species composition and relative abundance of copepods in Chilean fjords

We studied the species composition of copepods in the fjordregion, Isla Madre de Dios, Chile during October 1979. Fifteennew records for the fjords are cited. We found the antarcticcopepod Paraeuchaeta antarctica which is consistent with earlyrecords of other antarctic zooplankters in the area. The analysisof relative abundances shows that changes in dominance occuronly among four most abundant species of copepods.     

Sexual communication in copepods and rotifers

The problem of locating mates and identifying them as conspecifics is similar for Copepoda, Cladocera, and Rotifera since they are all relatively small animals moving in a large volume of water. Chemoreception is a potentially effective means of identifying mates in aquatic environments. In zooplankton, mate recognition systems based on chemoreception have evolved which can distinguish conspecifics from other species and can discriminate males from females. The evidence for the role of chemical signals in copepod mating is indirect, based on observations of mating behavior. The small size and limited metabolic capability of zooplankton, and high diffusion rates at 1–10 mm spatial scales, restrict the volume through which chemical signals can be effectively transmitted. An alternative to using diffusible molecules for sexual communication is to bind signal molecules to cell surfaces, allowing energetically costly molecules like proteins to serve as signals without their loss through diffusion. Contact chemoreception has been described in copepod and rotifer mating and perhaps represents a general solution to the problem of chemical communication by small zooplankters. The types of signals used, their mechanisms of transmission and reception, and their role in maintaining reproductive isolation among species has yet to be characterized for any aquatic invertebrate. In this review, I compare the methods used by copepods and rotifers for mate seeking and recognition, describe the behavioral evidence supporting the existence of chemical cues, and examine experiments describing the biochemical characteristics of the signal molecules. In copepods, male mate seeking behavior occurs without previous female contact, suggesting the reception of a diffusible signal. The signal molecule is small and lacks species specificity in the species investigated. Male rotifers do not respond to females from a distance. Mates are located by random male swimming and contact chemoreception of a species-specific signal. Mate recognition in both copepods and rotifers is based on contact chemoreception of a species-specific signal. The pheromones responsible are not known for copepods, but surface glycoproteins with pheromonal activity have been identified in rotifers. The structure of the rotifer sex pheromone has been probed by selective enzymatic degradation and lectin binding, electrophoretic characterization, and attachment to agarose beads to assess its biological activity. Glycoproteins play a key role in the sexual communication of some algal and ciliate species and have well characterized roles in cellular recognition phenomena like sperm-egg binding. The significance of these studies lies in their contribution to our understanding of zooplankton reproductive biology, the chemical ecology of male-female communication, the molecular basis of chemoreception in the aquatic environment, and the evolution of pre-mating reproductive isolating mechanisms in zooplankton.     

Directional Hydrodynamic Sensing by Free-Swimming Organisms

Many aquatic organisms detect the presence of moving objects in their environment, such as predators, by sensing the hydrodynamic disturbances the movements produce. The resultant water flow is readily detectable by stationary organisms, but free-swimming organisms are carried with the surrounding water and may not detect the bulk surrounding flow, which limits the available information about the source. We have developed a theory that clarifies what information is contained in disturbances generated by an attacking predator that is available to a free-swimming organism and might be extracted from local flow deformations alone. The theory shows that, depending on how well the deformations can be measured in space and time, an organism can reduce the range of possible locations, speeds, sizes, and arrival times of the predator. We apply the theory to planktonic copepods that have mechanosensory hairs along a pair of antennules. The study reveals the presence of “blind spots,” potential ambiguities in resolving from which of two sides a predator attacks, and whether it generates a bow wave or suction. Our findings lead to specific testable hypotheses concerning optimal escape strategies, which are helpful for interpreting the behavior of evasive prey and designing free-swimming robots with sensory capabilities.     

Diel changes in plankton and water chemistry in Wicken brickpit

In a flooded Fenland brickpit 3 metres deep a 24-hr study (supplemented by other observations in the field and in the laboratory) revealed marked changes with depth and time in oxygen concentration, pH, total carbon dioxide, ammonium, oxidised nitrogen, phosphate and silica; as well as changes in the rate of cell-division and the vertical distribution of phytoplankton (Dinobryon and Peridinium), and the feeding and vertical movement of zooplankton (copepods, Bosmina, Ceriodaphnia, Polyarthra and Keratella). Directional trapping of zooplankton revealed relationships between population density and the intensity of locomotory activity (a relationship subsequently supported by laboratory experiments), and between the rate of change of light intensity and the direction of swimming. Significant temporal segregation of the occupancy of a given level by zooplankters implies interspecific competition. Transient peaks in the concentrations of some nutrients near the surface are tentatively attributed to nutrient release by zooplankters that have fed at depth. Small-scale temporal and spatial heterogeneity of the type described here may help to explain the paradox of the plankton.These marked diel changes in water chemistry suggest that conclusions based on the analysis of single water samples should be viewed with caution.[/p]     

An experimental test of mate choice for red carotenoid coloration in the marine copepod Tigriopus californicus

Colorful ornaments are hypothesized to have evolved in response to sexual selection for honest signals of individual quality that provide information about potential mates. Red carotenoid coloration is common in diverse groups, and in some vertebrate taxa, red coloration is a sexually selected trait whereby mates with the reddest ornaments are preferred . Despite being widespread among invertebrates, whether red carotenoid coloration is assessed during mate choice in these taxa is unclear. The marine copepod Tigriopus californicus displays red coloration from the accumulation of the carotenoid astaxanthin. Previous research on copepods has shown that astaxanthin provides protection from UV radiation and xenobiotic exposure and that carotenoid production is sensitive to external stressors. Because of the condition dependency of the red coloration, we hypothesized that Tigriopus would use it as a criterion during mate choice. To test this hypothesis, we conducted trials in which males chose between females that were wild-type red (carotenoid-rich algae diet) or white (carotenoid-deficient yeast diet). To control for dietary differences and to isolate the effect of carotenoid coloration, we also presented males with restored-red females fed a carotenoid-supplemented yeast diet. We found that wild-type red females were weakly preferred over white females. After controlling for diet, however, we found that restored-red females were avoided. Our observations do not support the hypothesis that male copepods prefer the carotenoid coloration of females during mate choice. We hypothesize that algal-derived compounds other than carotenoids play a role in mate choice. Red coloration in copepods appears to be a condition-dependent trait that is not assessed during mating.     

The zooplankton of a small tropical reservoir (Solomon Dam,North Queensland)

This paper examines seasonal changes in the density and taxonomic composition of the zooplankton of a small tropical impoundment, in relation to factors of water temperature, food supply and reservoir flushing. The response of the zooplankton to management techniques designed to regulate the density of cyanobacteria in the dam are also considered. Cyclopoid copepods were the dominant zooplankters, although Cladocera became much more significant following the introduction of measures to control cyanobacteria. Planktonic Rotifera were a diverse but generally unimportant fraction of the total biomass, except following seasonal or management induced environmental perturbations, when the Rotifera often recovered most rapidly.     

Costs and Benefits of Opisthobranch Swimming and Neurobehavioral Mechanisms

After opisthobranch molluscs dislodge from the substrate duringonset of swimming, the ensuing flexion or undulatory motionsare usually not well oriented with respect to predators, preyor suitable substrate. Swimming motions are effective in launchinganimals off the substrate and elevating them into the watercolumn where they are primarily transported passively by ambientwaves and tidal currents. Both active swimming and passive transporton ambient currents may provide escape from predators, searchfor food and mates, and dispersal to new and potentially adaptivelocations. However, loss of contact with the substrate and launchinginto the water column may also bring a high cost in terms ofexposure to diverse risks. I illustrate several forms of opisthobranchswimming and describe their mechanisms and roles. In addition,adaptations of some opisthobranchs to reduce the risks of exposureto predators during swimming are suggested. These adaptationsinclude small size, transparency or inconspicuous color to reducepredation while swimming, and neurobehavioral mechanisms ofrheotaxis and geomagnetic sensitivity.     

Chemical, mechanical and visual cues in the vertical migration behavior of the marine planktonic copepod Acartia hudsonica

Recent experimental evidence in both marine and freshwater systemsindicates that predators can induce vertical migration behaviorin individual zooplankters, yet the specific cues by which zooplankterssense their predators appear to vary. In situ manipulation experimentswere carried out with enclosed populations of the marine planktoniccopepod Acartia hudsonica to re-examine the potential role ofchemical cues in the behavior of A.hudsonica, and to test explicitlyfor the role of mechanical or visual stimuli in triggering verticalmigration behavior in this species. Adult female copepods wereinduced to vertically migrate (descend) when exposed to fishmimics during the day, but no such response occurred when thecopepods were exposed to Fish mimics during the night. Moreover,copepods exhibited no changes in vertical distribution whenexposed to water which, having recently held a natural predator(the threespine stickleback, Gasterosteus aculeatus), was presumedto be laden with predator-produced chemical exudates. Predator-mediatedmechanical or visual cues, or a hierarchy of both, are responsiblefor eliciting vertical migration behavior in adult female A.hudsonica.These results, together with those of other investigations demonstratingthe inducing role of chemical exudates, indicate that the stimulieliciting vertical migration in zooplankton can be expectedto vary between species.     

The time course and frequency content of hydrodynamic events caused by moving fish,frogs, and crustaceans

Summary In the present study the time course and spectral-amplitude distribution of hydrodynamic flow fields caused by moving fish, frogs, and crustaceans were investigated with the aid of laser-Doppler-anemometry. In the vicinity of a hovering fish sinusoidal water movements can be recorded whose velocity spectra peak below 10 Hz (Fig. 2). Single strokes during startle responses or during steady swimming of fish, frogs, and crustaceans cause short-lasting, low-frequency (<10 Hz), transient water movements (Fig. 3). Low-frequency transients also occur if a frog approaches and passes a velocity-sensitive hydrodynamic sensor. In contrast, transient water movements caused by a rapidly struggling or startled fish or water motions measured in the wake of a slowly swimming (47 cm/s) trout can be broadbanded, i.e., these water movements can contain frequency components up to at least 100 Hz (Figs. 4, 5A, 6). High-frequency hydrodynamic events can also be measured behind obstacles submerged in running water (Fig. 5C). The possible biological advantage of the ability to detect high-frequency hydroynamic events is discussed with respect to the natural occurrence of high frequencies and its potential role in orientation and predator-prey interactions of aquatic animals.Abbreviations LDA laser Doppler anemometer     

Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus?

We investigated whether phosphorus limitations of primary producers propagate upwards through the food web, not only to the primary consumer level but also onto the secondary consumers’ level. A tri-trophic food chain was used to assess the effects of phosphorus-limited phytoplankton (the cryptophyte Rhodomonas salina) on herbivorous zooplankters (the copepod Acartia tonsa) and finally on zooplanktivores (the ctenophore Pleurobrachia pileus). The algae were cultured in phosphorus-replete and phosphorus-limited media before being fed to two groups of copepods. The copepods in turn were fed to the top predator, P. pileus, in a mixture resulting in a phosphorus-gradient, ranging from copepods having received only phosphorus-replete algae to copepods reared solely on phosphorus-limited algae. The C:P ratio of the algae varied significantly between the two treatments, resulting in higher C:P ratios for those copepods feeding on phosphorus-limited algae, albeit with a significance of 0.07. The differences in the feeding environment of the copepods could be followed to Pleurobrachia pileus. Contrary to our expectations, we found that phosphorus-limited copepods represented a higher quality food source for P. pileus, as shown by the better condition (expressed as nucleic acid content) of the ctenophore. This could possibly be explained by the rather high C:P ratios of ctenophores, their resulting low phosphorus demand and relative insensitivity to P deficiency. This might potentially be an additional explanation for the observed increasing abundances of gelatinous zooplankton in our increasingly phosphorus-limited coastal seas.     

How are the vertical migrations of copepods controlled?

Using Calanus finmarchicus (Gunnerus) as a model organism, a hypothesis is suggested to explain the diel and seasonal vertical migrations of herbivorous copepods in boreal and polar waters. The hypothesis is based on the following assumptions. Hungry copepods are assumed to react to food smell by increased swimming. High lipid content is assumed to turn the copepods upside down. Light avoidance is assumed to operate solely while the copepods are satiated. The following three major peaks in downflux of phytoplankton remains are assumed to reach 1000 m depth or more: pre- and post-spring bloom peaks and the autumn increase. A minor “afternoon peak” in short-range downflux of phytoplankton is also assumed to exist. The assumptions are used to explain the following main traits in copepod migrations. The afternoon increase in downflux of phytoplankton material induces upward swimming of hungry copepods. If satiated, light avoidance brings them down again at dawn. The late stages of many species of copepods accumulate large amounts of lipids and if the above assumptions are valid, they will be turned upside down and swim down if activated. During midsummer, the downflux does not reach deep water and the copepods are assumed to spend some time in midwater until they moult. Copepods moulting from stage V into female adults use up to half of their lipids to produce eggs, which are more anteriorly located. This is assumed to turn their bodies back into an upright position and the copepods are assumed to swim up to the surface again when they smell sinking phytoplankton remains. Fat copepods are assumed to follow the downflux of phytoplankton material down to diapause depths, especially at the end of the spring bloom and in autumn. It is assumed that enough lipids are used up during the diapause to turn the copepods into head-up position again. The smell of fast-sinking fecal pellets containing prebloom phytoplankton is assumed to bring the copepods up from diapause again in late winter. The probable implications for the survival of cod larvae are discussed.     

Distribution of zooplankton during opposite tide fluxes in the lagoon complex of Chelem, Yucatan, Mexico]

Zooplankton was surveyed in a tropical lagoon system of the northern coast of the Yucatan Peninsula in high tide, December (1998) and low tide, March 1999 (northerlies season). Zooplankton biomass was measured, zooplankters were counted, and copepods were identified and quantified. Despite the fact that both months were influenced by winds from the North, they showed a different salinity gradient which developed a particular structure of the zooplankton community. Biomass tended to be accumulated in certain areas apparently because of the high residence time of water in Chelem, the forcing effect of the northerlies, and of the tidal current. Biomass values suggest a relatively high secondary production when compared with other systems of the Yucatan Peninsula. The distribution of the copepods Acartia lilljeborgii and A. tonsa is related to saline conditions and tidal flow. The overall faunistic and hydrologic data suggest that even during a single climatic season, the zooplankton community shows strong changes due to mesoscale hydrological processes.     

The flow field around a freely swimming copepod in steady motion. Part I: Theoretical analysis

The three-dimensional flow field around a free-swimming copepodin steady motion was studiedtheoretically. This study was basedon coupling the Navier–Stokes equations with the dynamicequations for an idealized body of a copepod. To allow analyticalsolutions to the flow field, three simplifications were made:(a) to simulate the effect of the beating movement of the cephalicappendages, a force-field was added to the Navier–Stokesequations, (b) to linearize the problem, Stokes flow was used,and (c) to simplify the morphologies of the copepods, a sphericalbody shape was assumed. Analytical solutions were derived forfive steady motions: (1) hovering, (2) sinking, (3) upwardsswimming, (4) backwards swimming and (5) forwards swimming.The results show that thegeometry of the flow field around afreely swimming copepod varies significantly with the differentswimming behaviours. When a copepod hovers in the water, orswims very slowly, it generates a wide, cone-shaped flow field.In contrast, when a copepod sinks, or swims fast, the flow geometryis not cone-shaped, but cylindrical, narrow and long. Theseresults are consistent with published observations on live copepods.It is shown that the differences in the flow geometry with thedifferent swimming behaviours are due to the relative importancebetween the two factors in generating the flow field: the copepod'sswimming motion and the requirement to counterbalance the copepod'sexcess weight. The results also highlight the importance ofconsidering freely swimming copepods as self-propelled ratherthan as towed bodies. ‘Self-propelled’ means a freelyswimming copepod must gain thrust from the surrounding waterin order to counterbalance the drag force by water and its excessweight. Regardless of swimming behaviours and velocities, thefar-field velocity field decays to that of the velocity fieldgenerated by a point force of magnitude equal to the copepod'sexcess weight in an infinite domain. On the other hand, usingthe towed body model yields a flow field with much differentfar- and near-field flow characteristics. Hence, the towed bodymodel is inherently unable to reproduce fundamental characteristicsof the flow field around a freely swimming copepod.     

Abundance and Community Structure of Limnetic Zooplankters in Kumaun Lakes,India

The zooplankton compositions in the limnetic zones of two subtropical lakes, the Nainital and the Bhimtal (U.P., India) were more or less similar in terms of species composition. Numerically, zooplankters were abundant during the thermal stratification (summer-autumn) period and scarce during the over-turn (winter). The density of the zooplankton population reported from the eutrophic Lake Nainital was higher than in the oligotrophic Lake Bhimtal. Among the three groups studied copepods dominated over cladocerans and rotifers in both the lakes. The Shannon Weaver diversity was higher for Lake Bhimtal than for Lake Nainital. The community structure has also been discussed on the basis of crustacean species.