Escape behavior of Acartia hudsonica copepods during interactions with scyphomedusae

Calanoid copepods possess remarkable abilities to detect andescape from hydrodynamic disturbances, such as those createdby approaching predators. At the same time, a number of studiesin coastal ecosystems have suggested that gelatinous predators,including medusae in the Class Scyphozoa, exert top-down controlon copepod populations. Although prey escape behavior playsa critical role in predation models, we have relatively littleempirical data on how copepods respond to encounters with scyphomedusae.In this study, I used video to quantify encounter rates andescape behaviors of the copepod Acartia hudsonica during interactionswith two scyphomedusae, Aurelia aurita and Cyanea sp., in twoflow regimes. Escapes were complex, variable and effective.Fewer than 1% of encounters resulted in ingestion. Typically,A.hudsonica avoided contact by responding when predators remainedseveral body lengths (4 to 10 mm) distant and stringing togethermany escape jumps at submaximum velocities (33 to 59 mm s^–1).In addition, copepodite stages behaved passively—or failedto respond—following encounters with medusae more oftenthan did adults. Because escape behavior exhibited by A.hudsonicawas so variable, it is unlikely that medusae capture copepodsusing a single, quantifiable mechanism. A range of responseswithin populations and individuals may be the best strategyfor zooplankton faced with strong predation pressure from avariety of predators.     

Implications of the feeding current structure of Euchaeta rimana, a carnivorous pelagic copepod, on the spatial orientation of their prey

Many marine planktonic organisms create water currents to entrainand capture food items. Rheotactic prey entrained within thesefeeding currents often exibit escape reactions. If the directionof escape is away from the feeding current, the prey may successfullydeter predation. If the escape is towards the center of thefeeding current, the prey will be re-entrained towards its predatorand remain at risk of predation. The direction of escape isdependent on (i) the ability of the prey to escape in a directiondifferent than its pre-escape orientation and (ii) the orientationcaused by the interaction of the prey's body with the movingfluid. In this study, the change in orientation of Acartia hudsonicanauplii as a result of entrainment within the feeding currentof Euchaeta rimana, a planktonic predatory copepod, was examined,When escaping in still water, A.hudsonica nauplii were ableto vary their pre-escape direction by only 10. This allowsonly a limited ability to escape in a direction different thantheir pre-escape orientation. Analyses of the feeding currentof E.rimana show the flow speed to be most rapid in the centralregion with an exponential decrease in speed distally. In contrast,flow vorticity is minimal in the center of the feeding currentand maximal at 1.75 mm along the antennae. As a result, thedegree of rotation of the prey towards the center of the feedingcurrent shows a strong dependency on the prey's location withinthe feeding current. The feeding current of E.rimana rotatedthe prey 14 when near the center of the flow field and up to160 when located more distal in the feeding current Since theprey's escape abilities cannot compensate for the rotation dueto the flow, this mechanism will maintain the escaping preywithin the feeding current of their predator. Therefore, thefeeding current facilitates predatory copepods in capturingprey by (i) increasing the amount of water which passes overtheir sensors and through their feeding appendages and (ii)controlling the spatial orientation of their prey prior to escape.     

A method for in situ estimation of prey selectivity and predation rate in large plankton, exemplified with the jellyfish Aurelia aurita (L.)

A method to estimate predation rates of large predatory zooplankton, such as jellyfish and ctenophores, is outlined. Large plankton size allows direct visual tracking of the predator during the process of foraging. The presented method is novel in the sense that it measures predation rate of a specific individual plankton predator in situ.After prey has been evacuated from the gut of an individual predator, the predator is incubated in situ, and observed by SCUBA-divers who recapture the individual after a defined time. Given that this incubation time is shorter than prey digestion time, predation rate can be calculated as increase in gut content over time. Clearance rates for different prey can be calculated from predation rates and prey concentrations in the water, allowing accurate estimates of prey selectivity. Thus, the problem of unknown feeding history and feeding environment, which can otherwise be a problem in prey selectivity studies of in situ-captured predators, is circumvented. Benefits and limitations of the method are discussed.The method was applied to adult medusae of the common jellyfish Aurelia aurita. A large variation in number of captured prey was detected both among individual jellyfish and among the various oral arms and gastric pouches within individuals. Clearance rates varied strongly with prey type. The medusae selected large crustacean prey (cladocerans and copepods/copepodites) over echinoderm larvae and copepod nauplii. Prey distribution within the medusae indicates that both tentacles and oral arms were used as prey capturing sites. Food passage time from prey capturing organs to gastric pouches was estimated.     

In situ time budgets of the scyphomedusae Aurelia aurita, Cyanea sp., and Chrysaora quinquecirrha

The in situ behavior of three scyphomedusan species was videorecorded by scuba divers in natural daytime lighting with minimalinterference to the medusae. The mean percentage of time thatindividual medusae spent swimming ranged from 93 to 100%. Therewere no significant differences in the percent time spent swimmingbetween life stages of a species (ephyra, adult) or betweenspecies. The predominance of swimming activity by medusae indicatesthat swimming, and hence the creation of fluid motions responsiblefor prey entrainment and capture, plays a widespread functionalrole in feeding by scyphomedusae.     

Predator-induced diet vertical migration in a planktonic copepod

Predator evasion is the most commonly hypothesized reason fordiel vertical migrations undertaken by a wide variety of planktonicorganisms in lakes and seas, yet direct evidence remains elusive.We tested the predation hypothesis by exposing enclosed populationsof a marine copepod Acartia hudsonica to caged or free-rangingindividuals of their natural predator, the planktivorous fishGasterosteus aculeatus. After little more than a week, adultcopepods changed their vertical distribution and migration behaviordepending on the presence or absence of predation. Only free-rangingfish induced vertical migration in the copepod population. Cagedfish had no effect, indicating that vertical migration was nota simple chemically mediated response of copepods to the predator.Rather, copepods seemed to react to the presence of predatorsby other means, perhaps visual or mechanical stimuli, and toexhibit a downward escape response which, because encounterswith visually orienting fish occur chiefly in the daytime, effectivelylimited the copepods' occurrence in the upper water column tothe night-time hours. Alternatively, because fish imposed heavymortality on copepods, it is possible that selective predationaltered the proportions of individuals with fixed, geneticallydetermined migration behaviors. We suggest experiments to distinguishthese alternatives.     

Effects of Protoceratium reticulatum yessotoxin on feeding rates of Acartia hudsonica: A bioassay using artificial particles coated with purified toxin

Paralytic shellfish toxins produced by dinoflagellates are known to deter copepod grazing. Dinoflagellate species, including Protoceratium reticulatum, also produce disulfated polyether yessotoxins that were previously referred to as diarrheic shellfish toxins. However, the role of yessotoxins in predator–prey relationships is not yet clear. In the present study, the effects of purified yessotoxin (YTX) on feeding activities of Acartia hudsonica (Copepoda, Calanoida) were experimentally investigated. Polystyrene fluorescent microspheres (10 μm in diameter) colored bright blue or yellow-green were coated with cell extracts of P. reticulatum that do not produce yessotoxins. The bright blue microspheres were further coated with YTX, and the yellow-green microspheres were used as the reference. The microspheres were then given to the copepods separately or in combination to measure clearance rates and feeding selectivity. A. hudsonica was found to feed on the yellow-green microspheres without YTX at twice the rate of the bright blue microspheres with YTX. We also confirmed that microsphere color per se did not affect the feeding rates. The bright blue microspheres adsorbed 1.8–43.3 pg of YTX per microsphere, which is similar to the cell-specific yessotoxin content of toxic P. reticulatum found in natural environments. These results suggest that production of yessotoxin is advantageous for P. reticulatum by deterring predation by copepods.     

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.     

The effect of container size on the feeding rate of Heterocope septentrionalis, a freshwater predaceous copepod

The feeding rates of freshwater predaceous copepods have beenmeasured many times using enclosure experiments. Typically theseexperiments involve enclosing a known number of zooplanklonprey with a known number of predaceous copepods and determiningthe number of prey remaining after a set length of time. Variousfactors such as prey species and size have been shown to influencethe feeding rate of copepods. However, little attention hasbeen paid to the influence that container size may have on feedingrates. Using previously published data and some new data itwas found that container size has a major impact on the feedingrate of Heterocope septentrionalis, a predaceous freshwatercopepod common in North American arctic waters. In experimentswith Daphnia puiex, where container size varied from 0.3 to54 l (180 times), the measured feeding rate coefficient variedfrom –0.04 to –1.7 (42.5 times). Other prey speciesshowed similar changes, but the vulnerability of particularprey species to Heterocope predation remained consistent acrossthis range of expenmental containers. The reason for the containereffect is not known, but it is postulated that edge avoidanceby Heterocope may account for the observed change in feedingrate.     

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.     

Diel vertical migration in zooplankton: rapid individual response to predators

While diel vertical migration in zooplankton has been shownrecently to be a predator avoidance behavior, the mechanismby which predators induce and maintain such behavior has beendebated. We report results of an in situ predator manipulationexperiment during which enclosed populations of the marine planktomccopepod Acaraa hudsonica rapidly changed their vertical distributionand diel migration behavior depending on presence or absenceof the planktivorous fish Casterosteus aculeatus These resultspoint unambiguously to phenotypic behavioral plasticity of individualplanktonic prey, not, as previously hypothesized, population-geneticlevel behavioral changes caused by selective fish predation,as the mechanism underlying changes in diel vertical migrationin this copepod.     

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.     

Predator-limited population growth of the copepod Pseudocalanus sp.

The impact of predators on population growth of Pseudocalanussp. was investigated in Dabob Bay, Washington. Mortality ofPseudocalanus sp. was determined from stage-specific survivorship,from seasonal changes in mortality rates of adult males andfemales and from incidence of injuries to adult copepods. Theprincipal predators of adult Pseudocalanus were identified asthe predatory copepod Euchaeta elongata, the omnivorous euphausiidEuphausia pacifica and the chaetognath Sagirta elegans. Predatorattack rates - and prey mortality rates - are highly density-dependentand thus sensitive to prey dispersion in the water column, particularlyto layering in the vertical plane. Predation rates by the threeprincipal predators exceeded 100% of the recruitment rate toadult Pseudocalanus sp. beginning in early summer, thus restrictingpopulation growth. Planktivorous fish predation (by adult three-spinestickleback, Gasterosteus aculeatus, and juvenile chum salmon,Oncorhynchus keta) on Pseudocalanus sp. adults was estimatedto be two orders of magnitude lower than consumption rates bypredatory zooplankton, at a deep water station in July. Analysisof seasonal changes in prey ingested by Sagitta elegans revealedthat Pseudocalanus sp. was the major prey item of S. elegansin April (61.0% of prey) and in June (67.0% of prey), thereafterdeclining seasonally in importance. Predation by S. elegansvaried seasonally with changes in chaetognath stage structure,vertical distribution and diapause, not size structure alone.Although chaetognath recruitment and population growth appearto be directly coupled to the abundance of Pseudocalanus sp.,predation by S. elegans has little reciprocal impact on Pseudocalanussp. population growth; hence asymmetries may occur in the interaction of planktonic prey and predators.     

The importance of protozooplankton as prey for copepods in the coastal areas of the central Irish Sea

This study evaluates food supply for copepods, highlighting the trophic relationship between copepods and protozooplankton. To test the hypotheses that protozooplankton prey are capable of sustaining the copepod standing stock in the western Irish Sea, the taxonomic and size composition of these two groups and the size-specific predation of copepods on protozooplankton were investigated. Protozooplankton and copepod samples were collected off the southwest coast of the Isle of Man using 1.7 l Niskin water bottles and two nets (64 and 280 μm meshes), respectively. Copepod predation on protozooplankton was calculated using weight-specific clearance rates from the literature, considering the availability of prey that was accessible to a given size of copepod. Low protozooplankton biomass was dominated by small cells (<60 μm), and high copepod biomass was dominated by small species, which were more efficiently collected by a 64-μm mesh net. However, large copepods were only collected by a 280-μm mesh net, suggesting that the combination of the two nets provided a better estimate of copepod biomass. Predation by the copepod assemblage in the Irish Sea removed 1–47% and 0.5–22% of ciliates and dinoflagellates standing stock, respectively, resulting in 1–40% of the copepod feeding requirement per day. Contrary to our hypothesis, copepods could not meet their feeding requirements by grazing only on the microzooplankton prey (15–200 μm), and other food sources (i.e. nanoplankton) must be important additional dietary components to copepods in the Irish Sea. Handling editor: S. M. Thomaz     

Behavioral interactions between a cyclopoid copepod predator and its prey

Behavioral observations on the predatory interactions betweenMesocyclops edax and several different types and sizes of preyrevealed that prey size alone was less important than otherspecific morphological and behavioral characteristics of theprey in deterring successful predation by the copepod. The behavioralresponses of Bosmina and Asplanchna to an attacking copepodwere passive and consisted of a simple retraction of vulnerableswimming appendages which made the prey more difficult to grasp.Daphnia and Diaphanosoma on the other hand exhibited very activeswimming escape responses. Tropocyclops usually avoided M. edaxby fleeing before the larger predator could detect them. Thehard carapaces of Daphnia, Bosmina and Keratella were effectiveat reducing ingestion following capture by M. edax. The resultsof these behavioral observations were supported by enclosureexperiments in which the predator was offered a choice betweentwo prey simultaneously. Cyclopoid copepods are capable of successfullyattacking, capturing and ingesting prey organisms several timestheir own body length. Although size alone may influence thepreference of cyclopoid copepods on large and small individualsof the same or similar prey species, it is not a dependabledeterminant of the preference of cyclopoids on multispecificprey assemblages. ¹Present address: Department of Biology, Williams Hall No. 31,Lehigh University, Bethlehem, PA 18015, USA     

Planktonic predators and copepod abundance near the Dutch coast

Hypotheses that planktonic predators are responsible for thespring-summer decrease in copepod abundance and that the dominantpredator, Pleurobrachia pileus, is associated with high concentrationsof copepods were investigated at a station near the Dutch coast.Neither hypothesis was supported. Predators and copepods weresampled together with a 156 L ‘water box’ from lateApril through early July, including the season of P.pileus abundance.Using predators and copepods from the same box samples, hencefrom the same water parcel, feeding rates on copepod naupliiand copepodites + adults were measured onboard ship. Less than6% of the copepods, the sensitivity of the method, were removedper day. In additional shipboard feeding experiments net-caughtP.pileus were added to ambient copepod densities. By combiningwater volume cleared of copepods with ambient P.pileus densityin the sea, the predicted impact was 0–1.6% of copepodseaten per day from late April to early July. The hypothesisthat P.pileus associates with copepod concentrations was testedby comparing abundances of both groups from the same box samples.The correlations were not significant for any sample series.The ways measurement methods have restricted progress in understandingthe predatory impact of Pleurobrachia sp. are also considered.     

Predaceous feeding habits of Limnocalanus macrurus

Limnocalanus macrurus, a large, glacial-relict copepod, hasbeen assumed an omnivore or a herbivore; predaceous habits ofthe species are unknown. The predaceous feeding habits of Limnocalanusfrom Lake Michigan were studied in the laboratory using naturalprey. Predation rates were highest on copepod nauplii. Copepoditesof Diaptomus spp. and Cyclops spp. were preyed upon at lowerrates. Limnocalanus preyed selectively upon nauplii <300µm. Small cyclopoid copepodites (<–750 µm)were also selected over large copepodites. Experiments usingtwo prey types showed that nauplii were selected over all copepodites,and that no selectivity existed for either diaptomid or cyclopoidcopepodites. Predaceous feeding habits began in the fourth copepoditestage of Limnocalanus. Predaceous feeding rates of Limnocalanuschanged seasonally being highest in late spring and autumn andlowest in summer and early winter. Since Limnocalanus also feedson net-phytoplankton, predation rate changes may be relatedto changes in the relative abundance of large phytoplanktonand naupliar prey in nature. Limnocalanus predation may be animportant factor in structuring the zooplankton community. Present address: Great Lakes Research Division, University Michigan,Ann Arbor, MI 48109, USA     

Freshwater Copepods and Rotifers: Predators and their Prey

Three main groups of planktonic animals inhabit the limnetic zone of inland waters and compete for common food resources: rotifers, cladocerans and copepods. In addition to competition, their mutual relationships are strongly influenced by the variable, herbivorous and carnivorous feeding modes of the copepods. Most copepod species, at least in their later developmental stages, are efficient predators. They exhibit various hunting and feeding techniques, which enable them to prey on a wide range of planktonic animals from protozoans to small cladocerans. The rotifers are often the most preferred prey. The scope of this paper is limited to predation of freshwater copepods on rotifer prey. Both cyclopoid and calanoid copepods (genera Cyclops, Acanthocyclops, Mesocyclops, Diacyclops, Tropocyclops, Diaptomus, Eudiaptomus, Boeckella, Epischura and others) as predators and several rotifer species (genera Synchaeta, Polyarthra, Filinia, Conochilus, Conochiloides, Brachionus, Keratella, Asplanchna and others) as prey are reported in various studies on the feeding relationships in limnetic communities. Generally, soft-bodied species are more vulnerable to predation than species possessing spines or external structures or loricate species. However, not only morphological but also behavioural characteristics, e.g., movements and escape reactions, and temporal and spatial distribution of rotifer species are important in regulating the impact of copepod predation. The reported predation rates are high enough to produce top-down control and often achieve or even exceed the reproductive rates of the rotifer populations. These findings are discussed and related to the differences between the life history strategies of limnetic rotifer species, with their ability to quickly utilize seasonally changing food resources, and adjust to the more complicated life strategies of copepods.     

Copepod reaction to odor stimuli influenced by cestode infection

The cestode Schistocephalus solidus uses copepods as first andsticklebacks as second intermediate hosts. For transmission,an infected copepod has to be preyed upon by a stickleback.We used copepods of the species Macrocy albidus to test whetherinfected and uninfected copepods differ in their reaction totwo kind of simultaneously presented odors: odors of sticklebacksand odors of sticklebacks and conspecificz. By giving this choice,we attempted to force the copepods to make a trade-off betweenthe benefit of risk dilution and possible predator confusionand the costs of food competition and other disadvantages inducedby conspecifics. Within 1–8 h after last feeding, uninfectedcopepods clearly preferred the odors of conspeciflcs under thechemically simulated threat of predation. This was in contrastto the infected copepods, who tended to avoid the odor of conspecifics.When the time between experiment and last feeding varied, infectedcopepods showed an increas preference for fish water only (oravoided conspecthcs) with increasing hunger level This suggeststhat S. solidus benefits from hunger-induced behavioral changesof its copepod host by influencing its microhabitat selection.The same effect could be found in both sexes; however, it wassignificantly more pronounced in male than in female copepods.We propose several hypotheses that could explain the differencebetween the sexes in their infection-dependent microhabitatselection.     

The role of amino acids in the chemosensory swarming and feeding of marine copepods

Behavioural observations were made on two copepods, Eurytemoraherdmani and Acartia hudsonica, presented with 18 dissolvedL-amino acids the concentrations of which ranged from 10^–8M to 10^–2 M. The onset and duration of the swarming behaviourwere determined by the structure and concentration of a restrictednumber of molecules, which differed depending on the copepodspecies. Dicarboxylic amino acids were the most stimulatoryagent for E. herdmani, whereas A. hudsonica responded preferentiallyto aliphatic amino acids. Both the feeding and swarming of A.hudsonica could be induced by the same kind of molecules. Thethreshold sensitivity of the copepods appeared to be compatiblewith the natural concentrations of the dissolved free aminoacids measured at sea. These findings are discussed with referenceto the chemically mediated interactions between phytoplanktonand zooplankton.     

Trophodynamics of the plankton community at Dogger Bank: predatory impact by larval fish

The trophodynamics of a coastal plankton community were studied,focusing on fish larvae and their copepod prey. The major objectiveswere to describe distributional overlap and evaluate the predatoryimpact by larval fish. The study was carried out across DoggerBank in the North Sea, August-September 1991. Sampling transectscrossed tidal fronts off the Bank and plankton at all trophiclevels showed peak abundance within frontal zones. Also Verticallythere was a significant overlap in distributional patterns ofthe plankton. Seven species of fish larvae were abundant, ofthese sprat (Sprattus sprattus) dominated. The abundance ofone group of fish larvae peaked in the shallow water close tothe Bank, whereas other species, including sprat, were foundin deeper water. Prey preference and predation pressure of fishlarvae were assessed using information on prey sizes and growthrates of larvae and the copepod prey. We estimated larval removalof preferred prey sizes to 3–4% day^–1, counterbalancedby a 3–7% day^–1' replenishment from copepod productionand growth. Additional predation pressure on copepods by aninvertebrate predator was estimated to 1–3%day^–1.In conclusion, the dynamics of fish larvae and other zooplankterswere closely linked. At peak abundances of fish larvae (>35mg dry weight m^–2), the accumulated predation on specificsize ranges of copepods, exerted by larvae and other predators,could exceed the ability of copepod replenishment and intra-/interspecificcompetition among predators might take place.