Diel feeding pattern and prey selection of mesozooplankton on microplankton community

Mesozooplankton play an important role in transporting energy from microphytoplankton and microzooplankton to higher trophic levels. However there were few studies on the diel feeding patterns and prey selectivity of mesozooplankton. We conducted feeding experiments of mesozooplankton in the East China Sea to determine their respective diel feeding patterns on diatoms, ciliates and dinoflagellates, and to assess the contribution of these prey items to mesozooplankton diet. The results showed higher mesozooplankton grazing rates on ciliates and dinoflagellates than on diatoms at the day time, and the opposite pattern at the night time. A significant prey selection was observed, in which mesozooplankton positively selected ciliates and dinoflagellates during day and diatoms at night. The different grazing reactions of mesozooplankton toward each prey item might be related to the mobility of the prey. In all, microzooplankton (ciliates and dinoflagellates) provided the majority of the mesozooplankton carbon ingestion, even at a station dominated by small pennate diatoms. In particular, dinoflagellates are an important prey of mesozooplankton in the East China Sea and their contribution to the diet of mesozooplankton is unproportionate to their abundance.     

Seasonal and vertical distribution of the ciliated protozoa and micrometazoa in Kaštela Bay (central Adriatic)

Seasonal and vertical distribution of tintinnids, non-loricate ciliates and micrometazoa were studied in Kaštela Bay (central Adriatic Sea) throughout 1995. The species composition of tintinnids and copepods were studied as well. This is the first estimation of non-loricate ciliate biomass in the coastal area of the central Adriatic. Non-loricate ciliates were quantitatively the best represented ciliated protozoa, whereas nauplii were the most numerous micrometazoan organisms. Temperature affected the distribution of most micrometazoan components of the zooplankton and that of non-loricate ciliates. The temperature-dependent presence of individual size categories of non-loricate ciliates was also established. Apart from the interaction between microzooplankton groups, the influence of biotic factors, such as phytoplankton, bacteria, non-pigmented nanoflagellates (NNF) and mesozooplankton, was also discussed. The abundance of ciliates was controlled by both food supply (phytoplankton and NNF) and micrometazoan grazing. The results point to very complex trophic relationships within the planktonic community, suggesting that microzooplankton could be an important link between the microbial food web and higher trophic levels. Received in revised form: 8 November 2000 Electronic Publication     

The influence of mesozooplankton on phytoplankton nutrient limitation: a mesocosm study with northeast Atlantic plankton

We used marine phytoplankton from mesocosms seeded with different zooplankton densities to study the impact of mesozooplankton on phytoplankton nutrient limitation. After 7 d of grazing (copepod mesocosms) or 9 d (appendicularian mesocosms) phytoplankton nutrient limitation was studied by enrichment bioassays. After removal of mesozooplankton, bioassay bottles received either no nutrients, phosphorus or nitrogen alone, or a combination of nitrogen and phosphorus and were incubated for 2 d. Phytoplankton reproductive rates in the bottles without nutrient addition were calculated after correction for grazing by ciliates and indicated increasing nitrogen limitation with increasing copepod abundance. No nutrient limitation was found in the appendicularian mesocosms. The increase of nutrient limitation with increasing copepod density seems to be mainly the result of a trophic cascade effect: Copepods released nanoplankton from ciliate grazing pressure, and thereby enhanced nitrogen exhaustion by nanophytoplankton and reduced nitrogen excretion by ciliates. Nitrogen sequestration in copepod biomass, the mechanism predicted by the ecological stoichiometry theory, seems to have been a weaker effect because there was only little copepod growth during the experiment.     

Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary,USA

Microzooplankton grazing can have significant impacts on the distribution and abundance of phytoplankton, thereby influencing the frequency and duration of algae blooms. Observations of high ciliate abundances in the Suwannee River estuary, Florida, suggest a significant potential for top-down pressure on the phytoplankton community by microzooplankton. We examined the composition of the microzooplankton and determined grazing mortality losses for phytoplankton within the Suwannee River estuary from 2001 to 2002. Our results indicated grazing mortality rates of 1.4 d⁻¹, equivalent to a loss of up to 76% of phytoplankton standing crop and up to 83% of total daily primary production. The microzooplankton community was primarily composed of ciliates, dinoflagellates, and copepod nauplii. The densities of ciliates in the estuary were comparable to densities reported in highly eutrophic ecosystems (9,400–72,800 ciliates l⁻¹). Grazing pressure on small phytoplankton may be further enhanced because ciliates and small dinoflagellates have growth rates similar to those of phytoplankton, and therefore can keep up with surges in abundance. Handling editor: Judit Padisak     

Grazing impact of micro- and mesozooplankton during a spring situation in coastal waters off the Gironde estuary

The aim of this study was to characterize the grazing link betweenphytoplankton and zooplankton. Quantifying rates of phytoplanktonutilization by micro- and mesozooplankton is an attempt to understandthe control of phytoplankton populations in marine ecosystemsand the export flux of organic matter to the depths. Sampleswere taken in the plume of dilution of the Gironde estuary duringspring (May 1995). The mesozooplankton community was dominatedby the heterotrophic dinoflagellate Noctiluca scintillans andby copepods. Our estimates showed that on average, 26% of thetotal primary production was grazed daily by mesozooplankton.However, the pressure exerted by microzooplankton on the primaryproduction was estimated to be approximately four times higher.As a consequence, during this spring situation in the plumeof dilution of the Gironde estuary when small cells dominated,microzooplankton represented the most important grazing communityand could potentially control the growth of phytoplankton.     

Copepod growth and diatoms: insensitivity of <Emphasis Type="Italic">Acartia tonsa</Emphasis> to the composition of semi-natural plankton mixtures manipulated by silicon:nitrogen ratios in mesocosms

The feeding selectivity and the growth and reproductive success of the copepod Acartia tonsa have been studied in mesocosms fertilized at different Si:N ratios (0–1.75:1) and, therefore, at different compositions of the phytoplankton communities. Phytoplankton composition showed a strong response to nutrient ratios, with diatoms comprising >90% at Si:N ratios >1:1 of total biomass as opposed to <20% at the lowest ratio. A. tonsa strongly preferred feeding on motile prey (flagellates and ciliates) to feeding on diatoms. Nevertheless, diatoms comprised a substantial part of the diet at the highest Si:N ratios. A. tonsa egg production and the final (after 4 weeks) abundance of adults and copepodites showed no response to Si:N ratios while nauplii production slightly increased with Si:N ratios. It is concluded that the frequently reported deleterious effect of diatoms on copepod reproduction is rather unusual when copepods are confronted with a naturally diverse phytoplankton assemblage instead of clonal cultures in the laboratory.     

Phytoplankton blooms: a 'loophole' in microzooplankton grazing impact?

Phytoplankton size and relations between phytoplankton and microzooplankton(ciliates and heterotrophic dinoflagellates) biomass are analysedin 12 globally distributed areas. In view of the results, ahypothesis is posed where blooming species are those able toescape control by microzooplankton through a combination ofpredation avoidance mechanisms (e.g. larger size, colonies,spines, and toxic compounds) at the beginning of the bloom.Factors that help to enhance subsequent bloom development includepositive feedback from the poor nutritional status of the phototrophicprey which adversely affects predation, inter-microzooplanktongrazing and top–down grazing by mesozooplankton on microzooplankton.Blooming conditions are interpreted as physical or chemicalperturbations disrupting the predator–prey controls thatnormally operate at the level of the microbial loop, opening‘loopholes’ into which some phytoplankton speciespopulations can explode.     

Biological interactions in enclosed plankton communities including Alexandrium catenella and copepods: Role of phosphorus

A microcosm approach was used to test whether: a) growth under unbalanced nutrient conditions (varying N:P ratios) affected the susceptibility of a phytoplankton community including the dinoflagellate Alexandrium catenella (a paralytic shellfish toxin producer) to mesozooplankton grazing, and b) the potential effects of unbalanced nutrient conditions were mediated by changes in toxicity of A. catenella or by other mechanisms. The experimental setup consisted of fifteen 30 l microcosms, filled with water from the Barcelona Harbour and subjected to treatments combining nutrient inputs at three different N:P ratios (Redfield N:P ratio or nutrient-balanced, high N:P and low N:P), addition or omission of A. catenella (an estimated initial concentration of 38 A. catenella cells ml^− 1, a value typical for blooms in harbours of the Catalan coast), and selective addition of a cultured population of Acartia grani. P sufficiency had a strong positive effect on the growth of A. grani, both with or without A. catenella addition, presumably due to enhanced food quality of the prey community. The presence of this copepod resulted in lower concentrations of ciliates, A. catenella, and other dinoflagellates, suggesting active grazing by the copepods. No noxious effects of A. catenella on the copepods were detected at the relatively low cell concentrations of that dinoflagellate used in the experiment.     

REACTIVE OXYGEN METABOLISM IN THE TROPICAL BROWN ALGA DICTYOTA DICHOTOMA

There is a growing understanding that phagotrophic ciliates are often important members of aquatic communities in terms of their trophic role and mobilization of small cell production to higher consumers. As formidable consumers of small phytoplankton species they are likely to be also important in determining the community composition of the pico- and nanophytoplankton assemblages. Dilution method experiments were conducted during the winter and summer in the South Slough, an arm of the Coos Bay on the southern Oregon coast, to assess the impact of ciliate grazing on two size fractions of chlorophyll (0.2 to 5 mm and> 5 mm) and on the growth and abundance of specific phytoplankton groups, particularly cryptophytes and Synechococcus sp. The premise of the dilution technique is that grazers are diluted with their food and the observed rate of change in chlorophyll or phytoplankton abundance is linearly related to the dilution factor. Results from previous studies using the dilution technique have been given in terms of the grazing impact of microzooplankton on total chlorophyll. The findings of the research presented using a more rigorous application of the dilution method suggest that ciliates are differential in their grazing of phytoplankton, targeting small phytoplankton biomass and preying selectively on components of the assemblage that constitute this biomass.     

Seasonal phytoplankton responses to N:Si:P enrichment ratio in the Bizerte Lagoon (southwestern Mediterranean)

This study investigated the role of N, P and Si enrichments on phytoplankton in the Bizerte Lagoon (southwestern Mediterranean Sea, Tunisia) during March, June, August, October and December 2004. Polycarbonate bottles were enriched with different nutrients according to four treatments N:Si:P ratios [+NSi/-P (40:40:1), +P/-NSi (20:20:2,5), +NP/-Si (16:0:1) and +Si/-NP (16:32:1)] and incubated in situ during six days. Chl a and carbon biomass of phytoplankton varied significantly during the course of months, with the highest levels recorded in summer (4-4.4 microg Chl a L(-1) or 1126-1721 microg C L(-1)). Dinoflagellates dominated the initial phytoplankton communities, except in August, when diatoms represented a high fraction of microalgae (48%). Enrichment experiments induced significant increases in Chl a and in the final phytoplankton carbon biomasses. In summer (June/August), Si was the main limiting element for phytoplankton. Diatoms strongly responded to +Si/-NP and +NSi/-P enrichments and dominated the final phytoplankton communities (52-61%) in both treatments. Si played the most important role in the growth and development of diatoms. The biomasses and growth rates of dinoflagellates were significantly stimulated by +P/-NSi and +NP/-Si enrichments. After 6 days, dinoflagellates represented more than 70% of the total phytoplankton biomass in samples subjected to these treatments. Moreover, the addition of +P/-NSi increased the biomasses of several dinoflagellates. This suggests that dinoflagellates were mostly controlled by P availability. Unlike diatoms and dinoflagellates, flagellates showed weak responses to nutrient treatments during only some months of the year. The results showed that phytoplankton dynamics in the lagoon were influenced by nutrients in different manners.     

THE IMPACT OF DIFFERENTIAL GRAZING BY PHAGOTROPHIC CILIATES ON PHYTOPLANKTON BIOMASS AND COMMUNITY STRUCTURE

There is a growing understanding that phagotrophic ciliates are often important members of aquatic communities in terms of their trophic role and mobilization of small cell production to higher consumers. As formidable consumers of small phytoplankton species they are likely to be also important in determining the community composition of the pico‐ and nanophytoplankton assemblages. Dilution method experiments were conducted during the winter and summer in the South Slough, an arm of the Coos Bay on the southern Oregon coast, to assess the impact of ciliate grazing on two size fractions of chlorophyll (0.2 to 5 mm and> 5 mm) and on the growth and abundance of specific phytoplankton groups, particularly cryptophytes and Synechococcus sp. The premise of the dilution technique is that grazers are diluted with their food and the observed rate of change in chlorophyll or phytoplankton abundance is linearly related to the dilution factor. Results from previous studies using the dilution technique have been given in terms of the grazing impact of microzooplankton on total chlorophyll. The findings of the research presented using a more rigorous application of the dilution method suggest that ciliates are differential in their grazing of phytoplankton, targeting small phytoplankton biomass and preying selectively on components of the assemblage that constitute this biomass.     

Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton

Indoor mesocosms were used to study the combined effect of warming and of different densities of overwintering mesozooplankton (mainly copepods) on the spring development of phytoplankton in shallow, coastal waters. Similar to previous studies, warming accelerated the spring phytoplankton peak by ca. 1 day °C^?1 whereas zooplankton did not significantly influence timing. Phytoplankton biomass during the experimental period decreased with warming and with higher densities of overwintering zooplankton. Similarly, average cell size and average effective particle size (here: colony size) decreased both with zooplankton density and warming. A decrease in phytoplankton particle size is generally considered at typical footprint of copepod grazing. We conclude that warming induced changes in the magnitude and structure of the phytoplankton spring bloom cannot be understood without considering grazing by overwintering zooplankton.     

Mesozooplankton distribution patterns and grazing impacts of copepods and Euphausia crystallorophias in the Amundsen Sea, West Antarctica, during austral summer

The rapid melting of glaciers as well as the loss of sea ice in the Amundsen Sea makes it an ideal environmental setting for the investigation of the impacts of climate change in the Antarctic on the distribution and production of mesozooplankton. We examined the latitudinal distribution of mesozooplankton and their grazing impacts on phytoplankton in the Amundsen Sea during the early austral summer from December 27, 2010 to January 13, 2011. Mesozooplankton followed a latitudinal distribution in relation to hydrographic and environmental features, with copepods dominating in the oceanic area and euphausiids dominating in the polynya. Greater Euphausia crystallorophias biomass in the polynya was associated with lower salinity and higher food concentration (chlorophyll a, choanoflagellates, and heterotrophic dinoflagellates). The grazing impact of three copepods (Rhincalanus gigas, Calanoides acutus, and Metridia gerlachei) on phytoplankton was low, with the consumption of 3 % of phytoplankton standing stock and about 4 % of daily primary production. Estimated daily carbon rations for each of the three copepods were also relatively low (<10 %), barely enough to cover metabolic demands. This suggests that copepods may rely on food other than phytoplankton and that much of the primary production is channeled through microzooplankton. Daily carbon rations for E. crystallorophias were high (up to 49 %) with the grazing impact accounting for 17 % of the phytoplankton biomass and 84 % of primary production. The presence of E. crystallorophias appears to be a critical factor regulating phytoplankton blooms and determining the fate of fixed carbon in the coastal polynyas of the Amundsen Sea.     

Response of temperate microplankton communities to N:Si ratio perturbation

In order to study the effect of the nitrogen:silicon (N:Si)ratio on temperate microplankton food webs, mesocosm experimentswere conducted in Trondheim (Norway) using two different ratios(molar ratios of 1:1 and 4:1). With the exception of diatoms,the increase in abundance of all microbial groups [phototrophicnanoflagellates, autotrophic dinoflagellates, bacteria, heterotrophicnanoflagellates (HNAN), heterotrophic microflagellates and ciliates]was significantly greater in the high N:Si treatment. Midwaythrough the experiment, HNAN biovolume exceeded that of bacteriain the high N:Si treatment, indicating strong top-down grazingcontrol. Heterotrophic microflagellate biovolume exceeded ciliatebiovolume under both nutrient regimes. However, heterotrophicplankton failed to respond rapidly to increased diatom biomass.The heterotrophic:autotrophic biovolume ratio remained <0.1for the majority of the experiment, suggesting that, given similarnutrient concentrations and ratios, much of the autotrophicproduction would be lost from surface waters through diatomaggregation and sinking before the micrograzer community wasable to respond. Measured differences in diatom physiology betweentreatments are discussed with respect to nutritional qualityand consequences for planktonic grazers.     

Annual variability in ciliate community structure, potential prey and predators in the open northern Baltic Sea proper

Biomass of ciliates, bacteria and mesozooplankton, as well asbiomass estimates of phytoplankton from chlorophyll a values,were studied in the mixed layer of the northern Baltic Sea proper,between February and December 1998. Production of phytoplanktonand bacteria was measured, and production of ciliates and mesozooplanktonwas estimated. The phytoplankton spring bloom in late Marchwas dominated by diatoms and dinoflagellates. Ciliates had abiomass peak shortly after the spring bloom, while mesozooplanktonpeaked in July. Thus, the predation pressure on ciliates waslow in spring, and ciliates were major predators, potentiallyconsuming up to 15% of the primary production. In summer, therewas a shift from larger to smaller ciliates coinciding witha shift from larger to smaller primary producers, an increasein bacterial production, and also an increase in mesozooplanktonabundance, mainly copepods. Elevated mesozooplankton predationand selective removal of larger ciliate species and/or a shiftto smaller prey size presumably caused these changes. The potentialcarbon consumption from ciliates and mesozooplankton was highestin summer and autumn, reaching 55 and 40% of the primary productionin summer and autumn, respectively. Ciliates consumed twiceas much as mesozooplankton, thus acting as important regenerators.     

“Windows of opportunity” for dinoflagellate blooms: Reduced microzooplankton net growth coupled to eutrophication

Links between eutrophication, plankton community structure, microzooplankton grazing and dinoflagellate abundance were investigated in two tributaries of the Chesapeake Bay, the Choptank and Patuxent Rivers (MD, USA). Sampling and experiments were conducted during the spring of consecutive dry (below average freshwater flow) and wet (above average freshwater flow) years. During the wet year (2003), dissolved inorganic nitrogen, phytoplankton, and copepod biomass, but not microzooplankton abundance, were greater than in the dry year. In 2003, but not 2002, small cell size photosynthetic dinoflagellates were abundant and blooms occurred in both rivers. Average potential microzooplankton grazing pressure on small dinoflagellates was spatially and temporally variable, but was not significantly different between years. Our data suggest that the variability in microzooplankton grazing pressure provided “windows of opportunity” for net growth of dinoflagellates in response to nutrient loading. The lack of net population growth of micrograzers in response to increases in dinoflagellate prey allowed dinoflagellate blooms to reach relatively high densities, however grazing also appeared to be important in limitation or demise of some blooms. We hypothesize that uncoupling of micrograzer–prey dynamics was partly due to strong top-down control by copepods of microzooplankton in the proportionately more eutrophic year, and perhaps also due to inhibition of microzooplankton grazing/growth once dinoflagellate densities are high.     

Dinoflagellates and ciliates at Helgoland Roads, North Sea

A monitoring programme for microzooplankton was started at the long-term sampling station “Kabeltonne” at Helgoland Roads (54°11.3′N; 7°54.0′E) in January 2007 in order to provide more detailed knowledge on microzooplankton occurrence, composition and seasonality patterns at this site and to complement the existing plankton data series. Ciliate and dinoflagellate cell concentration and carbon biomass were recorded on a weekly basis. Heterotrophic dinoflagellates were considerably more important in terms of biomass than ciliates, especially during the summer months. However, in early spring, ciliates were the major group of microzooplankton grazers as they responded more quickly to phytoplankton food availability. Mixotrophic dinoflagellates played a secondary role in terms of biomass when compared to heterotrophic species; nevertheless, they made up an intense late summer bloom in 2007. The photosynthetic ciliate Myrionecta rubra bloomed at the end of the sampling period. Due to its high biomass when compared to crustacean plankton especially during the spring bloom, microzooplankton should be regarded as the more important phytoplankton grazer group at Helgoland Roads. Based on these results, analyses of biotic and abiotic factors driving microzooplankton composition and abundance are necessary for a full understanding of this important component of the plankton.     

Microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): II. Ciliates and dinoflagellates

The composition and ecological role of ciliates and dinoflagellates were investigated at one station in Kongsfjorden, Svalbard, during six consecutive field campaigns between March and December 2006. Total ciliate and dinoflagellate abundance mirrored the seasonal progression of phytoplankton, peaking with 5.8 × 10⁴ cells l⁻¹ in April at an average chlorophyll a concentration of 10 μg l⁻¹. Dinoflagellates were more abundant than ciliates, dominated by small athecates. Among ciliates, aloricate oligotrichs dominated the assemblage. A large fraction (>60%) of ciliates and dinoflagellates contained chloroplasts in spring and summer. The biomass of the purely heterotrophic fraction of the ciliate and dinoflagellate community (protozooplankton) was with 14 μg C l⁻¹ highest in conjunction with the phytoplankton spring bloom in April. Growth experiments revealed similar specific growth rates for heterotrophic ciliates and dinoflagellates (<0–0.8 d⁻¹). Food availability may have controlled the protozooplankton assemblage in winter, while copepods may have exerted a strong control during the post-bloom period. Calculations of the potential grazing rates of the protozooplankton indicated its ability to control or heavily impact the phytoplankton stocks at most times. The results show that ciliates and dinoflagellates were an important component of the pelagic food web in Kongsfjorden and need to be taken into account when discussing the fate of phytoplankton and biogeochemical cycling in Arctic marine ecosystems.     

Copepod grazing during an iron-induced diatom bloom in the Antarctic Circumpolar Current (EisenEx): I. Feeding patterns and grazing impact on prey populations

Feeding activity, selective grazing and the potential grazing impact of two dominant grazers of the Polar Frontal Zone, Calanus simillimus and Rhincalanus gigas, and of copepods < 2 mm were investigated with incubation experiments in the course of an iron fertilized diatom bloom in November 2000. All grazers were already actively feeding in the low chlorophyll waters prior to the onset of the bloom. C. simillimus maintained constant clearance rates and fed predominantly on diatoms. R. gigas and the small copepods strongly increased clearance and ingestion of diatoms in response to their enhanced availability. All grazers preyed on microzooplankton, most steadily on ciliates, confirming the view that pure herbivory appears to be the exception rather than the rule in copepod feeding. The grazers exhibited differences in feeding behavior based on selectivity indices. C. simillimus and R. gigas showed prey switching from dinoflagellates to diatoms in response to the phytoplankton bloom. All grazers most efficiently grazed on large diatoms leading to differences in daily losses for large and small species, e.g. Corethron sp. or Thalassionema nitzschioides. Species-specific diatom mortality rates due to grazing suggest that the high feeding activity of C. simillimus prior to and during the bloom played a role in shaping diatom population dynamics.     

Cascading predation effects of Daphnia and copepods on microbial food web components

1. We performed a mesocosm experiment to investigate the structuring and cascading effects of two predominant crustacean mesozooplankton groups on microbial food web components. The natural summer plankton community of a mesotrophic lake was exposed to density gradients of Daphnia and copepods. Regression analysis was used to reveal top–down impacts of mesozooplankton on protists and bacteria after days 9 and 15. 2. Selective grazing by copepods caused a clear trophic cascade via ciliates to nanoplankton. Medium‐sized (20–40 μm) ciliates (mainly Oligotrichida) were particularly negatively affected by copepods whereas nanociliates (mainly Prostomatida) became more abundant. Phototrophic and heterotrophic nanoflagellates increased significantly with increasing copepod biomass, which we interpret as an indirect response to reduced grazing pressure from the medium‐sized ciliates. 3. In Daphnia‐treatments, ciliates of all size classes as well as nanoflagellates were reduced directly but the overall predation effect became most strongly visible after 15 days at higher Daphnia biomass. 4. The response of bacterioplankton involved only modest changes in bacterial biomass and cell‐size distribution along the zooplankton gradients. Increasing zooplankton biomass resulted either in a reduction (with Daphnia) or in an increase (with copepods) of bacterial biovolume, activity and production. Patterns of bacterial diversity, as measured by polymerase chain reaction–denaturing gradient gel electrophoresis (PCR–DGGE), showed no distinct grouping after 9 days, whereas a clear treatment‐coupled similarity clustering occurred after 15 days. 5. The experiment demonstrated that zooplankton‐mediated predatory interactions cascade down to the bacterial level, but also revealed that changes occurred rather slowly in this summer plankton community and were most pronounced with respect to bacterial activity and composition.