Perception of inert particles by calanoid copepods: behavioral observations and a numerical model

High-resolution video showed freely swimming Diaptomus sicilisattacking and capturing inert 5O µm polystyrene beadsthat were outside the influence of the copepod feeding current.The beads were frequently more than half a body length awayand were attacked after the ‘bow wake’ of the movingcopepod displaced the bead away from the copepod. To investigatethe hypothesis that deformation of streamlines around the copepodand its first antennae stimulated the attack response, a finiteelement numerical model was constructed. The model describedthe fluid interactions between a large object approaching asmaller object in a laminar flow at Reynolds number 5, whichis characteristic of the fluid regime experienced by foragingcopepods. The model revealed that fluid velocity fluctuationsand streamline deformations arose in the region between thetwo objects as separation distance between the objects decreased.The video observations and the model results support the hypothesesthat chemoreception is not required for the detection and captureof large phytoplankton cells [Vanderploeg et ai, in Hughes,R.N. (ed.), Behavioral Mechanisms of Food Selection. NATO ASISeries G20, 1990; DeMott and Watson, /. Plankton Res., 13, 1205-1222,1991], and that swimming behavior plays an integral role inprey detection. ⁴Present address: Academy of Natural Sciences Estuarine ResearchCenter, 10545 Mackall Road, St Leonard, MD 20685, USA     

Colonization of the pelagic realm by calanoid copepods

The evolution of calanoid copepods probably extends back into the mid-Paleozoic. Environmental change from the Paleozoic through to the Tertiary is reviewed. Turbidity, water clarity, oxygen, pelagic primary production, and tectonically induced changes in the morphology of the oceans are probably all important drivers of calanoid evolution and their invasion of the pelagic realm. Current views of the phylogeny of the Calanoida are presented as well as a review of some recent work on metabolic potential, female genital system, and nervous system. It is hypothesized that ancestors of the Arietelloidea and Diaptomoidea invaded the water column in the Devonian at a similar time to the Ostracoda and that the ancestors of the Calanoidea–Clausocalanoidea, with their myelinated axons, arose in the Permian during the major deep ventilation of the ocean. Present day distributions of some Diaptomidae, Centropagidae, and Calanidae suggest that these families successfully came through the Jurassic/Cretaceous expansion of the oxygen minimum zone and the K-T boundary event. Some Arietelloidea and Clausocalanoidea became secondarily benthic and may have survived the K-T boundary event in this environment. It is postulated that some Clausocalanoidea reinvaded the water column (e.g. Clausocalanidae, Aetideidae, Phaennidae, Scolecitrichidae) in the Tertiary after finding refuge in deep, low oxygen water away from the sea surface. It is possible that these hypotheses may be testable using genetic information in the near future.     

Mass density contrast in relation to the feeding currents in calanoid copepods

Theoretical analyses show that positively buoyant copepods areable to generate feeding currents by adopting upside-down bodypositions and pushing water upward. Thus, the excess buoyancyacting on the copepods will be balanced and cone-shaped feedingcurrents generated to transport water to the capture areas.The intensities of the feeding currents, which can be measuredin the present modeling study by calculating the volumetricflux going through the capture areas, are proportional to themass density contrasts between the copepods and the ambientseawater. The mass density contrasts may vary spatially andtemporally depending on copepod body contents and on the propertiesof the seawater immediately surrounding them. We focus on thecase where the mass density contrast between a wax ester-richcopepod and its ambient seawater can vary strongly with depthbecause wax esters are more compressible and 6–10 timesmore thermally expansible than seawater. These theoretical analysesshow that the intensities of the feeding currents generatedby wax ester-rich copepods vary strongly with depth. Our conclusionsfrom these theoretical analyses need to be tested by directobservations. This paper is one of six on the subject of the role of zooplanktonpredator–prey interactions in structuring plankton communities.     

The calanoid copepods of the Nile system

At least 11 or 12 calanoid taxa occur in the Nile system. One species is typical of the river and of Lake Chad (Th. galebi); two are restricted to Lake Victoria (Th. galeboides, T. stuhlmanni), but both might be only subspecies to more widespread species. One is restricted to Lakes Edward and George (T. worthingtoni) but is a little known species. No calanoids are on record from Lakes Albert and Kyoga, while the species reported from Lake Turkana (T. banforanus) is out of range, and almost certainly represents an erroneous record. Among the remaining species, four are East-African, ranging from the southern tip of the continent to the Ethiopian plateau and the Nile valley (P. schultzei, Th. mixtus, T. kraepelini, T. cf orientalis), while two are Sahelian species that span Africa from east to west (M. mauretanicus, T. processifer et ssp.).Two new synonyms are introduced. One new subspecies (T. processifier friedae) is described from the Ethiopian plateau. It is suggested that Tropodiaptomus orientalis (Brady, 1886), the type species of its genus, should not be considered a nomen dubium, but should be redescribed on its type female(s) and on topotypical males from Sri Lanka.     

Lipid dynamics and feeding of dominant Antarctic calanoid copepods in the eastern Weddell Sea in December

Lipid content, fatty acid composition, and feeding activity of the dominant Antarctic copepods, Calanoides acutus, Calanus propinquus, and Metridia gerlachei, were studied at a quasi-permanent station in the eastern Weddell Sea in December 2003. During 3 weeks of the spring phytoplankton development, total lipid levels of females and copepodite stages V (CVs) of C. acutus were almost doubled. Meanwhile, only a slight increase in total lipid content occurred in M. gerlachei, and no clear trend was observed in lipids of C. propinquus females. The pronounced increase of lipids in C. acutus was due to an accumulation of wax esters. The proportion of wax esters in the lipids of M. gerlachei was clearly lower, while triacylglycerols played a more important role. In C. propinquus, triacylglycerols were the only neutral lipid class. There were no pronounced changes in the feeding activity of M. gerlachei, whereas the feeding activity of C. acutus had rapidly increased with the development of the phytoplankton bloom in December, which explains its rapid lipid accumulation. The combination of gut content and fatty acid trophic marker analyses showed that C. acutus was feeding predominantly on diatoms. The typical diatom fatty acid marker, 16:1(n-7), slightly decreased and the tracer for flagellates, 18:4(n-3), increased in females and CVs of C. acutus. This shift indicates the time, when the significance of flagellates started to increase. The three copepod species exhibited different patterns of lipid accumulation in relation to their trophic niches and different duration of their active phases. The investigations filled a crucial data gap in the seasonal lipid dynamics of dominant calanoid copepods in the Weddell Sea in December and support earlier hypotheses on their energetic adaptations and life cycle strategies.     

Sexual dimorphism in calanoid copepods: morphology and function

Mate location and recognition are essentially asymmetrical processes in the reproductive biology of calanoid copepods with the active partner (the male) locating and catching the largely passive partner (the female). This behavioural asymmetry has led to the evolution of sexual dimorphism in copepods, playing many pivotal roles during the various successive phases of copulatory and post-copulatory behaviour. Sexually dimorphic appendages and structures are engaged in (1) mate recognition by the male; (2) capture of the female by the male; (3) transfer and attachment of a spermatophore to the female by the male; (4) removal of discharged spermatophore(s) by the female; and (5) fertilization and release of the eggs by the female. In many male calanoids, the antennulary chemosensory system is enhanced at the final moult and this enhancement appears to be strongly linked to their mate-locating role, i.e. detection of sex pheromones released by the female. It can be extreme in calanoids inhabiting oceanic waters, taking the form of a doubling in the number of aesthetascs on almost every segment, and is less expressed in forms residing in turbulent, neritic waters. Mate recognition is a process where chemoreception and mechanoreception presumably work in conjunction. The less elaborate male chemosensory system in the Centropagoidea is counterbalanced by females playing a more active role in generating hydromechanical cues. This is reflected in females in the shape of the posterior prosomal margin, the complexity of urosomal morphology and the size of the caudal setae. Visual mate recognition may be important in the Pontellidae, which typically show sexual dimorphism in eye design. The most distinctive sexual dimorphism is the atrophy of the mouthparts of non-feeding males, illustrating how copepod detection systems can be shifted to a new modality at the final moult. In the next phase, the male captures the female using the geniculate antennule and/or other appendages. Three types of antennulary geniculations are recognized, and their detailed morphology suggests that they have originated independently. Grasping efficiency can be enhanced by the development of supplemental hinges. The scanty data on capture mechanisms in males lacking geniculate antennules are reviewed. It is suggested that the loss of the antennulary geniculation in many non-centropagoidean calanoids has evolved in response to increasing predator pressure imposed on pairs in amplexus. Spermatophore transfer and placement are generally accomplished by the modified leg 5 of the male. In some males, leg 5 consists of both a chelate grasping leg and a spermatophore-transferring leg, whereas in others, only the latter is developed. Tufts of fine setules/spinules and/or sclerotized elements on the terminal portion of the leg are involved in the transfer and attachment of the spermatophore. The configuration of gonopores, copulatory pores and their connecting ducts in the female genital double-somite is diversified in the early calanoid offshoots such as Arietellidae and Metridinidae, whereas in more derived groups, it is constant and invariable, with paired gonopores and copulatory pores located beneath a single genital operculum. The absence of seminal receptacles in most Centropagoidea limits the female's ability to store sufficient sperm for multiple egg batches, suggesting that repeated mating is necessary for sustained egg production. Discharged spermatophores are usually removed by the female leg 5 and/or specialized elements on other legs. In Tortanus (Atortus) Ohtsuka, which has rudimentary fifth legs in the female and complex coupling devices in the male, a spermatophore supposedly remains on the female urosome, since eggs appear to be released from a ventral opening of the spermatophore. The type of sexual dimorphism is closely related to habitat and biology. Some hyperbenthic families never show multiplication of aesthetascs on the male antennule, whereas families of the open pelagic realm such as the Aetideidae always have non-feeding males exhibiting secondary multiplication of antennulary aesthetascs. The various aspects and diversity of calanoid sexual dimorphism are herein considered in an evolutionary context.     

Photophobic responses of calanoid copepods: possible adaptive value

A genual pattern of photophobic responses has been observedwhich differs for calanoid copepods from freshwater, estuarineand oceanic environments. Using a video-computer system formotion analysis, the photophobic responses of light and darkadapted calanoid copepods were compared. Dark-adapted copepodswere exposed to 600 ms flashes of dim blue light at 5 s intervalswhich simulated the flashes of biolumines-cent marine zooplankton.Light-adapted copepods were exposed to 600 ms intervals of darknessat 5 s intervals to simulate the shadows of organisms passingoverhead. Four species of coastal marine copepods (Acartia hudsonica,Centropages hamatus, Pseudocalanus minutus and Temora longicornis)all showed photophobic responses to both flashes and shadows.These responses may have adaptive value to the copepods sincethey live in an environment with predators that are bioluminescentat night and cast shadows on their prey during the day (e.g.ctenophores and cnidarian medusae). Two species of oceanic copepods(Euchaeta marina, Pleuromamma abdominalis) showed strong photophobicresponses to flashes but no response to shadows. This may correspondto the abundance of bioluminescent predators on copepods inthe oceanic environment (fish, ctenophores, siphonophores, etc.)and their lack of exposure to the shadows of predators, sinceboth these species are rarely found in the euphoric zone duringthe day. Two species of freshwater copepods (Diaptomus sanguineus,Epishwa massachusettsensis) showed no similar photophobic responseto flashes of light. This lack of startle response may relateto the lack of bioluminescence in the freshwater environment.Freshwater copepods showed a weak photophobic response to shadows.The adaptive value of this behavior is unclear, however, sincethe responses seem to be too weak to function for escape, andthe dominant predators large enough to cast shadows (fish) tendto approach their prey laterally. ¹Present address: Marine Science Institute, University of Texasat Austin, Port Aransas, TX 78373–1267, USA     

Mediterranean marine copepods: basin-scale trends of the calanoid Centropages typicus

The Mediterranean Sea is located in a crossroad of mid-latitude and subtropical climatic modes that enhance contrasting environmental conditions over both latitudinal and longitudinal ranges. Here, we show that the large-scale environmental forcing is reflected in the basin scale trends of the adult population of the calanoid copepod Centropages typicus. The species is distributed over the whole Mediterranean basin, and maximal abundances were found in the north-western basin associated to oceanic fronts, and in the Adriatic Sea associated to shallow and semi enclosed waters. The peak of main abundances of C. typicus correlates with the latitudinal temperature gradient and the highest seasonal abundances occurred in spring within the 14–18°C temperature window. Such thermal cline may define the latitudinal geographic region where C. typicus seasonally dominates the >200 μm-sized spring copepod community in the Mediterranean Sea. The approach used here is generally applicable to investigate the large-scale spatial patterns of other planktonic organisms and to identify favourable environmental windows for population development.     

Predation on ciliates by freshwater calanoid copepods: rates of predation and relative vulnerabilities of prey

• 1 The susceptibility of ciliates in a mesotrophic lake to predation by Epischura lacustris, Diaptomus minutus and D. pygmaeus was assessed during summer. Oligotrichs, particularly Strobilidium velox (c. 43 μm), were removed efficiently by adult copepods and contributed substantially to the diet of female D. minutus. The presence of approximately 1,6 adult Epischura 1-^?1, or sixteen adult female Diaptomus 1-^?1, could halt the growth of S. vechx populations in summer.
• 2 Factors affecting the rate at which copepods prey on ciliates were examined in experiments with D. pygmaeus and cultured ciliates. Rate of predation on S. velox, the preferred species, became saturated at 5 S. velox ml^?1 (45ngCml^?1) and did not change with a 10-fold increase in alternative algal food.
• 3 Behavioural differences among ciliates, and the presence of other ciliates, contributed to differences in ciliate susceptibility to predation and suggest reasons why rates of removal of ciliates are not related to ciliate size.
• 4 By feeding selectively, at high rates, calanoids may suppress populations of some ciliates and thereby influence microzooplankton community structure.

     

The role of turbulent diffusion for copepods with feeding currents

The encounter rate between predator and prey is frequently modeledin terms of the ‘swept volume’ associated with therelative velocity of the two organisms and an appropriate cross-sectionalarea. For the copepods which use feeding currents, an alternativeconceptual model of the process is that the food particles arediffusing towards the predators. Their feeding currents trapthe prey (even though they are well beyond the range of eithervisual or chemical detection) and entrain them towards theirwaiting arms. The predators thus benefit from the turbulentmotion and diffusion, even though much of it is due to motionswith scales significantly larger than their body's size. Thefeeding currents serve to dramatically increase the flux offood.     

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.     

Spatio-temporal distribution and production of calanoid copepods in the central Baltic Sea

The aim of our study was the exploration of species-specificdistribution and production patterns of dominant copepods inthe Central Baltic Sea (Bornholm Basin). Spatio-temporal distribution,egg and secondary production were studied by means of net-samplingand egg production experiments from April to August 1999. Verticaland horizontal distribution patterns appeared to be linked witheach other and were primarily species-dependent. Both Acartiaspp. and Temora longicornis preferentially inhabited the upper30 m of the water column and the shallower marginal regionsof the Bornholm Basin. In contrast, the C4–5 and C6 ofPseudocalanus spp. preferentially inhabited the halocline region(50–70 m) and the deep central part of the area. Observeddifferences in horizontal distribution among these three copepodsappear to result from different depth preferences and depth-dependentwater circulation patterns. Egg production rates (EPR) clearlyexhibited seasonal differences with maximum EPR in May and minimumEPR in July. Mean EPR was significantly different between species,being highest in Acartia spp. and lowest in Pseudocalanus spp.The variability in EPR was related to differences in hydrographyand modelled food environment.     

The distribution of calanoid copepods in the plankton of Wisconsin Lakes

Zooplankton communities from 499 lakes were examined for calanoid copepod species. Limnocalanus macrurus and Senecella calaloides are confined to Lakes Michigan, Superior and one inland lake each. Eurytemora affinis has recently become established in the coastal waters of Lakes Michigan and Superior. Epischura lacustris is present in the summer plankton of a wide variety of lake types. Aglaodiaptomus leptopus is sensitive to fish predation and confined to small lakes without fish. Leptodiaptomus ashlandi is restricted to Lakes Michigan and Superior, but L. sicilis is also found in some inland lakes. Leptodiaptomus minutus is a boreal species found mostly in lakes of the far north. Skistodiaptomus oregonensis is the most commonly occurring calanoid and seems well adapted to lakes of the meso-to low eutrophic types. Skistodiaptomus pallidus is also generally distributed throughout the state, but less common than oregonensis and adapted to more eutrophic lakes. Leptodiaptomus siciloides and A. clavipes are western species, adapted to eutrophic lakes, which are expanding their ranges eastward, aided by cultural eutrophication.     

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.     

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.     

Expression of serotonin and enkephalins in calanoid copepods (Crustacea): an immunohistochemical study

Copepods are the main metazoan component of zooplankton, interms of both the number of species and biomass. Thus, theyhave a key role in pelagic food webs; but curiously, nothingis known of the neuroendocrine substances involved in theirphysiological processes. In higher crustaceans, especially theDecapoda, the role of such molecules in different physiologicalprocesses (motility, feeding, reproduction, day-night migrationsand so on) has been well explored; so, we have mapped expressionsites of some of these substances to provide a better understandingof copepod physiology. Serotonin and, for the first time, leucine-and methionine-enkephalin were detected in copepods using immunofluorescencetechniques. Serotonin has mainly been identified in the centralnervous system acting probably as a neurotransmitter, notablyin the control of the escape reflex. In contrast, enkephalinsare only present in peripheral organs such as the naupliar eye,gut and shell glands. This localization suggests that opioidsare involved in visual function and reproductive and digestiveprocesses. In memory of Professor Jacques Mazza, an eminent copepodologist.     

Filtering and feeding rates of cyclopoid copepods feeding on phytoplankton

The algal biomass ingested by omnivorous cyclopoid copepods (Cyclops kolensis and C. vicinus) was measured by two methods in the hypertrophic Heiligensee in Berlin (West Germany). The clearance and ingestion rates inferred from measurements of natural populations of ¹⁴C labelled phytoplankton were compared with those obtained from chlorophyll a determinations using the presence/absence method (observed chlorophyll a content of natural lake phytoplankton with and without addition of cyclopoids). Both methods gave similar results. Nevertheless, the radio tracer method is preferred, mainly because the short feeding duration excludes high variations in both the food composition and food concentration that limit the presence/absence method.     

On the reorientation of non-spherical prey particles in a feeding current

Potentially, non-spherical prey can be re-oriented in a flowfield and impact on the predator's feeding structures in a non-randommanner. Herein, we quantify a process whereby this passive reorientationoccurs, and present a model that predicts the orientation ofa spheroidal prey as a function of its shape, size and the characteristicsof the fluid flow. For a radial flow field, elongated prey tendto align with their long axis parallel to streamlines. Thistheory is well supported by our results from a laboratory studyof cylindrical particles in a siphon flow. The model is extendedto a more realistic representation of copepod feeding currents.In this context, the spatial scale over which this process isactive is proportional to