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.     

Copepod Foraging on the Basis of Food Nutritional Quality: Can Copepods Really Choose?

Copepods have been considered capable of selective feeding based on several factors (i.e., prey size, toxicity, and motility). However, their selective feeding behaviour as a function of food quality remains poorly understood, despite the potential impact of such a process on copepod fitness and trophodynamics. In this study, we aimed to evaluate the ability of copepods to feed selectively according to the nutritional value of the prey. We investigated the feeding performance of the calanoid copepod Acartia grani under nutritionally distinct diets of the dinoflagellate Heterocapsa sp. (nutrient-replete, N-depleted and P-depleted) using unialgal suspensions and mixtures of prey (nutrient-replete vs. nutrient-depleted). Despite the distinct cell elemental composition among algal treatments (e.g., C:N:P molar ratios) and the clear dietary impact on egg production rates (generally higher number of eggs under a nutrient-replete diet), no impact on copepod feeding rates was observed. All unialgal suspensions were cleared at similar rates, and this pattern was independent of food concentration. When the prey were offered as mixtures, we did not detect selective behaviour in either the N-limitation (nutrient-replete vs. N-depleted Heterocapsa cells) or P-limitation (nutrient-replete vs. P-depleted Heterocapsa cells) experiments. The lack of selectivity observed in the current study contrasts with previous observations, in which stronger nutritional differences were tested. Under normal natural circumstances, nutritional differences in natural prey assemblages might not be sufficiently strong to trigger a selective response in copepods based on that factor alone. In addition, our results suggest that nutritional quality might depend not only on the growing conditions but also on the inherent taxonomical properties of the prey.     

Capture mechanisms used by the lobate ctenophore, Mnemiopsis leidyi, preying on the copepod Acartia tonsa

Although the lobate ctenophore Mnemiopsis leidyi is an influentialplanktonic predator, the mechanisms enabling it to capture itscharacteristically wide range of prey have not been systematicallyexamined. We recorded interactions between free-swimming M.leidyiand two stages (nauplii, adults) of the calanoid copepod Acartiatonsa in order to determine a mechanistic explanation of thisfeeding process. Prey encounter with Mnemiopsis involved twodifferent processes. The first depended on fluid motions createdby the nearly continuous beating of cilia lining the four auricles.These cilia created a low-velocity flow in which A.tonsa naupliiwere entrained (94% of naupliar encounters) and transportedpast the oral lobes onto the tentillae (oral tentacles). Thenauplii, although capable of rapid escape responses, generallyappeared to be insensitive to the current in which they werecarried. The second process relied upon the collision of swimmingprey with the inner surfaces of the oral lobes and was not obviouslyinfluenced by the auricular feeding currents. Adult A.tonsawere rarely entrained in the auricular flow, but, instead, propelledthemselves into contact with the oral lobes (97% of adult encounters).Both prey capture processes functioned simultaneously. The synergisticfunctioning of these processes probably explains the broad patternsof prey ingestion found by in situ studies of Mnemiopsis feeding.     

Foraging tactics and prey-selection patterns of omnivorous and carnivorous calanoid copepods

The foraging tactics and prey-selection patterns of omnivorous and carnivorous calanoid copepods are reviewed. Calanoid foraging tactics are envisioned as falling along several closely coupled continua reflecting swimming behavior, feeding behavior, and dietary habit. The consequences of these foraging tactics on prey-selection patterns are explored in the context of a graphical model. It is hypothesized that the prey-selection patterns of calanoid copepods are determined, to a large extent, by calanoid foraging tactics and the size relationships of predator and prey.     

Perceptive performance and feeding behavior of calanoid copepods

The goal of this study was to determine variables associatedwith calanoid feeding behavior, and thus, to improve our understandingof the basics of calanoid feeding rates. These variables includedperiods and frequency of appendage motion, rates of cell clearance,distance at which a copepod first reacts to a cell which iseventually captured, and rate of water flow through the areacovered by the motions of a copepod's feeding appendages. Theeffects of these variables on feeding rates were determinedfor copepodids and adult females of the calanoid copepod Eucalanuspileatus at phytoplankton concentrations covering the rangeencountered by this species on the south-eastern shelf of theUSA. Our results indicate that the distance at which E.pileatusperceives phytoplankton cells increases {small tilde}2-foldas food concentrations decrease from 1.0 to 0.1 mm³ l^–1.These results lead us to hypothesize that this is due to increasedsensitivity of chemosensors on the copepods' feeding appendages.This 2-fold increase in perceptive distance amounts to a near4-fold increase in perceived volume which is close to the 6-foldincrease in volume swept clear (VSC) from 1.0 to 0.1 mm³ l^–1of Thalassiosira weissflogii. We assume that the increases inVSC by planktonic copepods, when food levels are below satiation,are largely a function of the sensory performance of the individualcopepod.     

A comparison of the effects of prey and non-prey neighbours on foraging rates of Epischura nevadensis (Copepoda: Calanoida)

SUMMARY. 1. Adults of the calanoid copepod, Epischura nevadensis , aggregate in situ near the thermocline in Lake Tahoe, California-Nevada. together with adults of another species of calanoid copepod, Diaptomus tyrelli and juveniles of both species. With a series of laboratory predation and algal clearance trials, we show that foraging rates of adult E. nevadensis are determined not only by the density of co-occurring potential prey (small copepods), but also by the presence of co-occurring non-prey neighbours (large, adult copepods). These effects occur at densities and in zooplankton assemblages found naturally, emphasizing the ecological importance of neighbours other than prey on zooplankton feeding.
2. Neighbours are distinguished primarily by size. Although predation rates increase linearly with the densities of small copepods. both algal clearance and predation rates decrease in the presence of large copepods. We also show, with a field predation experiment using small enclosures, that adults are size selective within species and that Diaptomus are selected over conspecifics of the same size.
3. We hypothesize that by reducing foraging rates in the presence of large zooplankton. E. nevadensis avoids predators and reduces predation risk at the cost of reduced energy consumption.     

Effect of prey size on vulnerability of copepods to predation by the scyphomedusae Aurelia aurita and Cyanea sp.

A growing number of studies correlate changes in zooplanktonpopulations with abundance of medusae, but we cannot yet explainor predict the specific factors driving these interactions.This study demonstrates that the size of copepods has a significantinfluence on their vulnerability to predation by scyphomedusae.This finding is important because prey size, independent ofbehavior, has been neglected in theoretical models of predationby medusae. In experiments in a planktonkreisel, we used liveand heat-killed prey (Acartia hudsonica adults and copepodites)to separate the effects of copepod size and behavior on feedingrates by two medusae (Aurelia aurita and Cyanea sp.). Resultsrevealed that: differences in copepod size had a significantimpact on feeding rates, and thus small size can provide a refugefrom predation; behavior of adults diminished the liabilityassociated with larger size; and medusae with different morphologiesingested A.hudsonica at similar rates. Other experiments demonstratedthat medusae digested copepods at different rates based on preysize and predator species, findings that have implications forall future laboratory and field studies that assess feedingby scyphomedusae. Finally, this study illustrates how laboratorystudies serve as critical supplements to field observations.The effect of prey size on feeding rates can be confounded bydifferences in prey behavior, yet explains why small copepodswere typically ingested at relatively low rates by medusae.Size was clearly a dominant factor influencing copepod vulnerabilityacross scyphomedusan species, even those with very differentmorphologies. Future work should focus on the mechanisms ofsize selection, or the factors influencing contact and retentionrates.     

Factors affecting feeding selectivity of visual predators on the copepod Acartia tonsa: locomotion,visibility and escape responses

Visual predation by fish on copepods involves prey encounter, attack and capture; during any of these processes prey selection can occur. Developmental changes in copepods, including increases in swimming speed, size and image contrast increase the encounter rate and distance at which they can be detected by predators. Copepods compensate for this increase vulnerability with age through diel vertical migration and improved escape capabilities. This study quantifies the changes in swimming speed and movement pattern with developmental stage of the copepod Acartia tonsa, using a video-computer system for motion analysis. Changes in visible size and image contrast with developmental stage were quantified under simulated natural illumination conditions using a video based image analysis system. The escape responses of the naupliar stages of the copepod Acartia tonsa were quantified in response to a stationary pipette sucking in water at a constant speed. Accurate quantification of the parameters that affect feeding selectivity of planktivorous fish will provide the basis for evaluation of their relative importance in future studies.     

Top‐down regulation of filamentous cyanobacteria varies among a raptorial versus current feeding copepod across multiple prey generations

1. Although considered a key functional trait, little is known about how zooplankton feeding mode affects top‐down regulation of phytoplankton communities. Indeed, copepods are expected to promote the dominance of toxic phytoplankton by selective removal of their edible competitors; however, empirical evidence comparing the effect among calanoid and cyclopoid copepods is lacking.
2. We compared the top‐down effects of two copepods with contrasting feeding modes—the calanoid Notodiaptomus iheringi (current feeder) and the cyclopoid Thermocyclops decipiens (ambush feeder) — on the relative and absolute biomass of the filamentous cyanobacterium Raphidiopsis raciborskii co‐cultured with the nutritious eukaryotic phytoplankton Cryptomonas obovata in a week‐long laboratory assay.
3. The current feeder had a stronger top‐down effect on the biomass of both prey throughout the experiment, with mass‐specific clearance rates 3–5× higher than ambush feeder. By the end of the experiment, the current feeder significantly reduced cyanobacteria biomass compared to controls while the ambush feeder did not. During the week‐long experiment, the current feeder switched from grazing on edible prey to cyanobacteria as the former became less abundant.
4. Contrary to expectation, neither of the copepod species promoted cyanobacterial dominance by the end of the experiment. This is because both grazers, but especially the current feeder, initially increased but subsequently decreased the relative contribution of cyanobacteria to total phytoplankton biomass. Moreover, both copepods decreased the length of cyanobacteria filaments by c. 70%
5. Current feeders can switch from edible prey to cyanobacteria when the abundance of shortened filaments surpasses the abundance of edible prey. While top‐down regulation of phytoplankton can be stronger for current feeding copepods, ambush feeding copepods can have a significant role during blooms by shortening cyanobacterial filaments. Hence, the broader role of contrasting copepod feeding traits on phytoplankton communities merits further study.

     

Selective feeding of Arctodiaptomus salinus (Copepoda, Calanoida) on co-occurring sibling rotifer species

1. Using two‐ and three‐dimensional video recordings, we examined the steps involved in predation that lead to the differential vulnerability of three sympatric rotifer sibling species (Brachionus plicatilis, B. ibericus and B. rotundiformis) to a co‐occurring, predatory, calanoid copepod (Arctodiaptomus salinus). 2. Brachionus rotundiformis, the smallest prey tested, was the most vulnerable with the highest encounter rate, probability of attack, capture and ingestion, and the lowest handling time. 3. Comparison of our results with those of a previous study shows that A. salinus is a more efficient predator than a co‐occurring cyclopoid copepod (Diacyclops bicuspidatus odessanus) feeding on these same rotifer species. However, despite its higher capture rates, A. salinus seems to be less selective than D. b. odessanus based on attack distances and prey handling times. 4. The differential vulnerability to both calanoid and cyclopoid copepod predation can help explain the coexistence and seasonal succession of these co‐occurring rotifer species.     

Differences in feeding activity between females and males of Temora longicornis

We have studied experimentally in the laboratory the behavioural responses of females and males of the calanoid copepodTemora longicornis and their encounter probability with the alga Rhodomonas. Both sexes of this calanoid copepod adapted their motion velocity and style of swimming in reaction to the presence of prey. Their mean velocity, as well as the probability of high velocity values, increased in the presence of the algae. Moreover, the time spent in swimming activity increased, reflecting a possible adaptation in order to facilitate encounter with prey. Females were more sensitive to the presence of food: mean velocities showed a 40 % increase for males, from control to food conditions, whereas for females the increase was 240 %. This result was confirmed using several indicators: net-to-gross displacement ratio, probability density functions, and symbolic dynamics. This may indicate that female T. longicornis are more attracted by food than males.     

Acanthodiaptomus denticornis another omnivorous calanoid copepod: description of its mouth appendages and feeding experiments on animal prey

The mouthpart morphology of the freshwater calanoid copepod Acanthodiaptomus denticornis was examined with optical microscopy. The mouthparts have sharp teeth and stout appendages with clawlike setae, typical of omnivorous calanoid mouthpart morphology. Observation of the buccal aperture with Scanning Electron Microscopy shows a large opening permitting feeding on prey as large as Keratella cochlearis. These observations agree with our feeding experiments which show that A. denticornis feed on K. cochlearis.     

A model of the predatory impact of larval marine fish on the population dynamics of their zooplankton prey

A simulation model of the population dynamics of two speciesof calanoid copepods (Calanus.r pacificus and Pseudocalanussp.) was forced with predation pressure from a genetic, hypotheticalpopulation of larval marine fish. Results of the model are sensitiveto changes in parameters describing the dynamics of both predatorand prey populations, including initial numbers, fecundity,growth, mortality, size of prey organisms and feeding selectivityof the predators; the relative importance of these parametersis tested by way of a brute-force sensitivity analysis. Usingresults from recent ichthyoplankton surveys in Dabob Bay, WA,USA, the model was also forced with predation from populationsof larval Pacific herring (Clupea harengus pallasi) and Pacificwhiting (Merluccius productus). Results of the various simulationruns lead to the conclusion that marine fish larvae can significantlyimpact the population dynamics of their calanoid copepod prey,but that the magnitude of this impact is highly dependent onspecies-specific values of various population parameters.     

Copepod feeding in the ocean: scaling patterns,composition of their diet and the bias of estimates due to microzooplankton grazing during incubations

Here, we report insights from the compilation and analysis of data on marine calanoid copepod feeding rates in the ocean. Our study shows that food availability and body weight are major factors shaping copepod feeding rates in the field, with a relatively minor role of temperature. Although the maximal feeding rates of copepods that are observed in the field agree with the well-known 3/4 of body size scaling rule for animals, copepod feeding in the oceans is typically limited and departs from this rule. Ciliates and dinoflagellates appear to be highly relevant in the composition of copepod diets, and this represents an indirect increase in the flux of primary production that is likely to reach the upper trophic levels; this contribution is higher in the less productive systems and may help to explain accounts of proportionally higher standing stocks of copepods supported per unit of primary producer biomass in oligotrophic environments. Contrary to common belief, diatoms emerge from our dataset as small contributors to the diet of copepods, except in some very productive ecosystems. We have also evaluated the bias in the estimation of copepod grazing rates due to within-bottle trophic cascade effects caused by the removal of microheterotrophs by copepods. This release of microzooplankton grazing pressure accounts for a relevant, but moderate, increase in copepod grazing estimates (ca. 20–30%); this bias has an effect on both the carbon flux budgets through copepods and on our view of their diet composition. However, caution is recommended against the indiscriminate use of corrections because they may turn out to be overestimates of the bias. We advise that both uncorrected and corrected grazing rates should be provided in future studies, as they probably correspond to the lower and upper boundaries of the true grazing rates.     

Chemoreception and the deformationof the active space in freely swimming copepods: a numerical study

A three-dimensional alga-tracking, chemical advection–diffusionmodel was used to calculate the deformation of the active spacesurrounding an alga entrained within the flow field around afreely swimming copepod. From the model, the advance warningtime resulting from the copepod's chemo-reception of the entrainedalga was quantified, and copepod chemoreception capability comparedfor several different swimming behaviors: hovering in the water,swimming slowly (swimming upward, swimming backward and swimmingforward), swimming fast (swimming upward, swimming backwardand swimming forward) and sinking (with the anterior pointingupward or downward). The results show that when it hovers orswims slowly, a copepod can use chemoreception to remotely detectindividual algae entrained by the flow field around itself.In contrast, a fast-swimming copepod is not able to rely onchemoreception to remotely detect individual algae. The possibilityof a free-sinking copepod using chemoreception to detect algalparticles is also indicated. It is shown that advection by thefluid motion dominates over diffusion in transporting the chemicalsignals inside the active space to the location of a copepod'schemoreceptors. The feeding current structure for a hoveringcopepod is described. It is suggested that the feeding currentstructure and re-routing or re-orienting response by a copepodin response to its antennule or other cephalic appendage inputsallow the copepod to capture the food particles that would otherwisepass outside its capture area and increase the amount of foodcaptured.     

Generation time of Acanthocyclops robustus in relation to food availability and temperature in a shallow eutrophic lake

The generation time of the predatory cyclopoid copepod Acanthocyclops robustus was estimated on 11 occasions during the years 1980 to 1982 in Alderfen Broad. In a multiple regression model, generation time was found to be uncorrelated with temperature, positively correlated (p < 0.05) with the densities of Bosmina longirostris and rotifers, and negatively correlated (p < 0.001) with the density of nauplii of the calanoid copepod Eudiaptomus gracilis. It is suggested that generation time was determined largely by the availability of calanoid nauplii as prey, even though these constituted only 2% of zooplankton standing biomass.     

The flow field around a freely swimming copepod in steady motion. Part II: Numerical simulation

Three-dimensional, numerical simulations of the flow field arounda freely swimming model-copepod were performed using a finite-volumecode. The model copepod had a realistic body shape representedby a curvilinear body-fitted coordinate system. The beatingmovement of the cephalic appendages was replaced by a distributedforce field acting on the water ventrally adjacent to the copepod'sbody. In the simulations, we took into account that freely swimmingcopepods are self-propelled bodies through properly couplingthe Navier–Stokes equations with the dynamic equationfor the copepod's body. Flow fields were calculated for fivesteady motions: (1) hovering, (2) sinking, (3) upwards swimming,(4) backwards swimming and (5) forwards swimming. The numericalresults confirm the conclusions drawn from the theoretical analysisusing Stokes flow models by Jiang et al. [in a companion paper(Jiang et al., 2002a)] for a spherical copepod shape and showthat the geometry of the flow field around a freely swimmingcopepod varies significantly with the different swimming behaviours.When a copepod hovers in the water, or swims very slowly, itgenerates a cone-shaped and wide flow field. In contrast, whena copepod sinks, or swims fast, the flow geometry is not cone-shaped,but cylindrical, narrow and long. The relationships betweencopepods' swimming behaviour and body orientation, hydrodynamicconspicuousness, energetics as well as feeding efficiency werediscussed, based on the simulation data. It is shown that thebehaviour of hovering or swimming slowly is more energeticallyefficient in terms of relative capture volume per energy expendedthan the behaviour of swimming fast, i.e. for a same amountof energy expended a hovering or slow-swimming copepod is ableto scan more water than a fast-swimming one. The numerical resultsalso suggest that the flow field generated by a fast-swimmingcopepod enables the copepod to use mechanoreception to perceivethe food/prey and therefore increases the food concentrationin the swept volume and that the flow field around a free-sinkingcopepod favours the copepod's mechanoreception while minimizingthe energy expense, so that the energy budget can still be maintainedfor both cases.     

Predation on the Invasive Copepod,Pseudodiaptomus forbesi,and Native Zooplankton in the Lower Columbia River: An Experimental Approach to Quantify Differences in Prey-Specific Feeding Rates

Invasive planktonic crustaceans have become a prominent feature of aquatic communities worldwide, yet their effects on food webs are not well known. The Asian calanoid copepod, Pseudodiaptomus forbesi, introduced to the Columbia River Estuary approximately 15 years ago, now dominates the late-summer zooplankton community, but its use by native aquatic predators is unknown. We investigated whether three species of planktivorous fishes (chinook salmon, three-spined stickleback, and northern pikeminnow) and one species of mysid exhibited higher feeding rates on native copepods and cladocerans relative to P. forbesi by conducting `single-prey’ feeding experiments and, additionally, examined selectivity for prey types with `two-prey’ feeding experiments. In single-prey experiments individual predator species showed no difference in feeding rates on native cyclopoid copepods (Cyclopidae spp.) relative to invasive P. forbesi, though wild-collected predators exhibited higher feeding rates on cyclopoids when considered in aggregate. In two-prey experiments, chinook salmon and northern pikeminnow both strongly selected native cladocerans (Daphnia retrocurva) over P. forbesi, and moreover, northern pikeminnow selected native Cyclopidae spp. over P. forbesi. On the other hand, in two-prey experiments, chinook salmon, three-spined stickleback and mysids were non- selective with respect to feeding on native cyclopoid copepods versus P. forbesi. Our results indicate that all four native predators in the Columbia River Estuary can consume the invasive copepod, P. forbesi, but that some predators select for native zooplankton over P. forbesi, most likely due to one (or both) of two possible underlying casual mechanisms: 1) differential taxon-specific prey motility and escape responses (calanoids > cyclopoids > daphnids) or 2) the invasive status of the zooplankton prey resulting in naivety, and thus lower feeding rates, of native predators feeding on invasive prey.     

Vulnerability of Daphnia middendorffiana to Parabroteas sarsi predation: the role of the tail spine

The predaceous calanoid copepod Parabroteas sarsi and Daphniamiddendorffiana co-exist in South Andes ponds. Daphnia middendorffianajuveniles have a tail spine with negative allometric development.A series ofexperiments was carried out with tailed and tail-removedjuveniles of three different instars. In all cases tested, feedingrates were significantly higher on tail-removed prey. Directobservations showed a higher frequency of unsuccessful attackson spined juveniles when compared with tail-removed juveniles.The proportion of dorsal attacks also increased in spined juveniles.Prey total length was a much better predictor of feeding ratethan prey body size. Three groups of juveniles with equal totallength, but differentage, body size and biomass, showed no significantdifferences in their vulnerability to predation.     

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.