Emily Clare Roberts
email: e.roberts@swansea.ac.uk

Emma Claire Wootton

Keith Davidson

Hae Jin Jeong

Christopher D Lowe

David J S Montagnes

Jin

Feeding in the dinoflagellate Oxyrrhis marina: linking

Keywords: Feeding, Grazing, Ingestion, Phagocytosis, Oxyrrhis, Flagellate, Dinoflagellate Feeding, Grazing, Ingestion, Phagocytosis, Oxyrrhis, Flagellate, Dinoflagellate

INTRODUCTION

It is now recognised that protists dominate grazing activities in aquatic microbial food webs [START_REF] Sherr | Significance of predation by protists in aquatic microbial food webs[END_REF][START_REF] Sherr | Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea[END_REF] and are the main source of phytoplankton mortality in marine ecosystems, typically accounting for 60 to 70% of daily phytoplankton consumption [START_REF] Calbet | Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems[END_REF]). Thus, there has been an impetus to understand factors controlling feeding by planktonic protists and interpret their environmental consequences (e.g. Davidson et al., this issue). Although field-based feeding experiments provide valuable estimates of in situ grazing (e.g. [START_REF] Calbet | Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems[END_REF]), the extent to which feeding behaviour can be interpreted using this approach is limited by the difficulties associated with low cell concentrations, the presence of multiple species, and the control of other variables [START_REF] Montagnes | Selective feeding behaviour of key free-living protists: avenues for continued study[END_REF]. Consequently, many aspects of protist feeding have used laboratory-based studies on model species (see [START_REF] Montagnes | Selective feeding behaviour of key free-living protists: avenues for continued study[END_REF].

The heterotrophic dinoflagellate, Oxyrrhis marina (15-40 µm) is the most frequently used marine protist predator in laboratory-based feeding experiments. Since the initial observations of [START_REF] Kent | A Manual of the Infusoria, Including a Description of all Known Flagellate, Ciliate, and Tentaculiferous Protozoa, British and Foreign and an Account of the Organization and Affinities of the Sponges[END_REF], [START_REF] Barker | The culture and physiology of marine dinoflagellates[END_REF], and [START_REF] Droop | Phagotrophy in Oxyrrhis marina Dujardin[END_REF], O. marina has been employed extensively in feeding experiments due to its ease of culture, wide distribution, and tolerance to a range of environmental conditions (Lowe et al., this issue-b). Although it is not typically found in open waters (Watts et al., this issue), O. marina is both a raptorial and intercept feeder (see below) and is, therefore, representative in its feeding behaviour of many planktonic protists. Thus, O. marina has been used as a model to develop new methodologies to study feeding, including the use of live fluorescently-stained prey [START_REF] Premke | Predation on heterotrophic flagellates by protists: Food selectivity determined using a live-staining technique[END_REF][START_REF] Martin-Cereceda | Easy visualization of the protist Oxyrrhis marina grazing on a live fluorescently labelled heterotrophic nanoflagellate[END_REF], dual radioisotope-labelled prey [START_REF] Lessard | Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a dual-label radioisotope technique[END_REF], acidotrophic probes [START_REF] Carvalho | Acidotropic probes and flow cytometry: a powerful combination for detecting phagotrophy in mixotrophic and heterotrophic protists[END_REF], fatty acid biomarkers and compound-specific stable isotope techniques [START_REF] Pond | Monitoring microbial predator-prey interactions: an experimental study using fatty acid biomarker and compound-specific stable isotope techniques[END_REF]. Other studies incorporating O. marina have enabled interpretation of the relevance of chemoattractants, chemorepellents, and chemical defence within aquatic food webs (e.g. Strom et al., 2003a,b;[START_REF] Adolf | Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum[END_REF][START_REF] Tillmann | Allelochemical interactions and shortterm effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists[END_REF]. The effect of physical factors on feeding, including temperature, turbulence, and light have also been investigated [START_REF] Havskum | Effects of small-scale turbulence on interactions between the heterotrophic dinoflagellate Oxyrrhis marina and its prey, Isochrysis sp[END_REF][START_REF] Jakobsen | Circadian cycles in growth and feeding rates of heterotrophic protist plankton[END_REF][START_REF] Lowe | There are high levels of functional and genetic diversity in Oxyrrhis marina[END_REF][START_REF] Kimmance | Do temperature-food interactions matter? Responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina[END_REF][START_REF] Hartz | Investigating the ecological role of cell signaling in free-living marine heterotrophic protists[END_REF]. Finally, O. marina has been used extensively as a model predator to investigate selective feeding on different prey species (e.g. [START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF][START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF][START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF][START_REF] Davidson | The role of prey nutritional status in governing protozoan nitrogen regeneration efficiency[END_REF] and on prey of varying nutritional quality (e.g. [START_REF] Flynn | Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina. II. Release of nonprotein amines and feces during predation of Isochrysis[END_REF]Flynn et al., 2006).

Despite O. marina being a popular model organism (Montagnes et al., this issue), there remains a poor understanding of the mechanisms involved in its feeding behaviour.

Here we examine 'what' O. marina feeds on and 'how' it feeds. We then provide directions for future studies to link observed behaviour with feeding mechanisms, specifically to interpret the underlying factors driving prey selectivity. Oxyrrhis marina demonstrates remarkable versatility in its prey preferences [START_REF] Droop | The role of algae in the nutrition of Heteramoeba clara Droop, with notes on Oxyrrhis marina Dujardin and Philodina roseola Ehrenberg[END_REF][START_REF] Dodge | Fine structure of the dinoflagelate Oxyrrhis marina III[END_REF]. At the lower end of the size spectrum O. marina can grow on bacteria (<1 µm) and small algae, including Nannochloris oculata (2-4 µm) and Micromonas pusilla (1-2 µm) [START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF][START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF][START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF]. However, O. marina feeds optimally and achieves higher growth rates on small flagellates ≥4 µm [START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF][START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF][START_REF] Jeong | Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp[END_REF][START_REF] Jeong | Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers[END_REF]. Although research has often focussed on 'herbivorous' grazing activities (e.g. [START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF], O. marina also feeds on heterotrophic flagellates including Cafeteria sp. (3-4 µm), Goniomonas amphinema (4-5 µm), Pfiesteria piscicida (7-14 µm), and Stoekeria algicida (11-17 µm) (Jeong et al., 2007a,b;[START_REF] Martin-Cereceda | Easy visualization of the protist Oxyrrhis marina grazing on a live fluorescently labelled heterotrophic nanoflagellate[END_REF] in addition to photosynthetic flagellates such as Isochrysis galbana (4-5 µm) and Dunaliella primolecta (6-8 µm) [START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF][START_REF] Wootton | Biochemical prey recognition by planktonic protozoa[END_REF]. At the larger end of the prey size spectrum, O. marina can feed on protist species as large as itself; e.g. Cricosphaera elongata (20-30 µm) [START_REF] Droop | The role of algae in the nutrition of Heteramoeba clara Droop, with notes on Oxyrrhis marina Dujardin and Philodina roseola Ehrenberg[END_REF][START_REF] Dodge | Fine structure of the dinoflagellate Oxyrrhis marina. II: The flagellar system[END_REF] and is a well documented cannibal [START_REF] Martel | Morphological controls on cannibalism in a planktonic marine phagotroph[END_REF]. Oxyrrhis marina has even been observed "attacking" amphipods that are moulting or have just moulted (Gaines and Elbrächter, 1987). Although O. marina can feed on cells >20 µm, in contrast to other naked dinoflagellates such as Gyrodinium spirale, its optimum prey size is smaller than that of itself [START_REF] Hansen | Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale[END_REF][START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF]Davidson et al., this issue). Finally, in addition to nutrition obtained through phagotrophy, O. marina can survive through the uptake of dissolved organic molecules in the laboratory and may be able to use this mechanism in saprobic environments (see Lowe et al., this issue-b). The diverse diet of O. marina allows researchers to use this species as a versatile model. Like many grazers, O. marina exhibits a typical type II functional response (see [START_REF] Turchin | Complex population dynamics: a theoretical/empirical synthesis[END_REF] that can be represented by Eq. 1

Functional response

(1) where I is ingestion rate, I max is the maximum ingestion rate, k is the half saturation constant, and p is the prey concentration. A number of studies have determined functional responses for O. marina, and here we provide a brief summary of these responses (Fig. 1, Table 1). The shape of responses and the maximum ingestion rate may vary depending on prey species, but also between different studies of the same species (possibly due to different experimental conditions such as acclimation of the predator to prey concentrations; e.g. [START_REF] Tarran | Aspects of the grazing behaviour of the marine dinoflagellate Oxyrrhis marina[END_REF].

Carbon:chlorophyll a ratios are known to be quite variable [START_REF] Davidson | Relationships between photopigments, cell carbon, cell nitrogen and growth rate for a marine nanoflagellate[END_REF][START_REF] Montagnes | Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton[END_REF]. However, if we assume an 'average' value of 50 [START_REF] Sherr | Capacity of herbivorous protists to control initiation and development of mass phytoplankton blooms[END_REF] we find that much of the data presented in Fig. 1 are at chlorophyll a concentrations >20 mg chlorophyll a m -3 (1000 ng C ml -1 ). These chlorophyll concentrations would be typical of a dense phytoplankton bloom and hence there is a need to better determine functional responses at prey concentrations more representative of in situ abundances, if researchers are concerned with how O. marina behaves under conditions typical of open waters (note though that O. marina may rarely experience such conditions as it is not typically found in open waters, Watts et al. this issue). Davidson et al. (this issue) review the use of functional responses in mathematical models. They report that O. marina is typically represented by a type II functional response, which may be modified to account for other abiotic and biotic factors such as temperature and prey quality. Often, O. marina ingests its prey to near extinction (Fig. 1, Table 1).

However, significant prey thresholds may occur for some species of microzooplankton; e.g. [START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] and [START_REF] Flynn | Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina. II. Release of nonprotein amines and feces during predation of Isochrysis[END_REF] report prey thresholds of ~1 x 10 5 cells ml -1 for I. galbana being ingested by O. marina. Furthermore, Davidson et al. (1995a) found it necessary to use a modified type II response to account for such thresholds (see Table 2 in Davidson et al., this issue). There is, therefore, a need to better understand the existence of factors governing prey thresholds and to improve our parameterization of the functional response at lower prey concentrations.

SELECTIVE FEEDING BY OXYRRHIS MARINA

Although O. marina consumes a variety of prey, it has distinct feeding preferences. Here we shall consider the implication of experiments examining prey selectivity in this species.

Selective feeding on artificial particles

Using artificial particles, O. marina has been shown to discriminate between prey, based on size, biochemical composition, and charge [START_REF] Hammer | The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate)[END_REF][START_REF] Hammer | New biocompatible tracer particles: use for estimation of microzooplankton grazing, digestion, and growth rates[END_REF][START_REF] Wootton | Biochemical prey recognition by planktonic protozoa[END_REF]. For instance, ingestion rate is up to four times higher on 4 µm beads compared to 1 µm beads [START_REF] Hammer | The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate)[END_REF] although identical abundances of 4 µm and 1 µm beads were used, increasing encounter probability with 4 µm beads). Oxyrrhis marina can also discriminate against artificial particles with a high surface charge, including carboxylate and silicate beads [START_REF] Hammer | The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate)[END_REF] and can distinguish between beads with different surface biochemical composition, showing a significant preference for beads coated with mannose-BSA over N-acetylgalactosamine-BSA [START_REF] Wootton | Biochemical prey recognition by planktonic protozoa[END_REF]. Although O. marina ingests artificial particles, it prefers live prey [START_REF] Hammer | The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate)[END_REF][START_REF] Wootton | Biochemical prey recognition by planktonic protozoa[END_REF]. Therefore, even though artificial prey provides a useful tool to elucidate some aspects of feeding behaviour, there are still unrecognised signals that live prey supply to induce capture. Numerous studies have investigated prey selectivity of O. marina grazing on other protists (e.g. [START_REF] Sieburth | Acrylic acid and "antibiotic" principle in Phaeocystis blooms in Antarctic waters[END_REF][START_REF] Barlow | Grazing and degradation of algal pigments by marine protozoan Oxyrrhis marina[END_REF][START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF][START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF][START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF]. Comparison between these studies is difficult due to differences in experimental design, including variations in incubation condition and duration [START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF][START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF][START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF]. Differences in the initial prey and predator abundance, biovolume, and biomass, further complicate comparisons. For example, the majority of feeding experiments presented in [START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF] used different biovolumes of prey mixtures and relatively short incubation times (48 h), with high predator concentrations. [START_REF] Hansen | Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells[END_REF] accounted for differences in prey concentration by applying the Chesson-index, as described by [START_REF] Chesson | The estimation and analysis of preference and its relationship to foraging models[END_REF] for use in selection experiments with changing prey densities. They concluded that O. marina grazes selectively on larger prey species such as Rhodomonas sp. and Tetraselmis suecica (with equivalent spherical diameters >7 µm), relative to smaller species including Emiliania huxleyi, Isochrysis galbana, Micromonas pusilla, and Nannochloris sp. (with equivalent spherical diameter of 1-5 µm). Selection for the larger cells within each species was also observed. In contrast, [START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] noted that selective feeding occurred on Phaeodactylum tricornutum, I. galbana, and Dunaliella tertiolecta by monitoring cell abundance, carbon, and nitrogen over longer time periods (10 d). Maximum ingestion rates based on abundance varied between prey species, with higher ingestion rates on P. tricornutum and I. galbana, relative to the larger species D. tertiolecta. However, on a cell nitrogen basis similar ingestion rates occurred for all three prey species. Prey selectivity experiments conducted by [START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF] biovolume of prey equal to its own cell volume [START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF]. When confronted with all three prey species, O. marina fed preferentially on D. primolecta but did not discriminate between I. galbana and M. pusilla. Comparison of these studies illustrates the difficulty of drawing general conclusions regarding prey selectivity and highlights the need for coordinated studies with comparable methodologies in future.

Prey selectivity between species

In studies of prey selectivity between species, it is difficult to determine the prey parameters that underpin selective feeding. Prey size, motility, cell surface properties, and the release of dissolved chemical cues (including chemoattractants, chemorepellents, and toxins) vary between different prey species. Experimentally controlling and manipulating these variables is challenging, and, at this point, it is difficult to interpret how prey parameters affect feeding preference of heterotrophic protists in general. However, given the tractability of O. marina as an experimental organism (Lowe et al., this issue-b), there is clearly a good opportunity to progress our understanding of prey selectivity mechanisms based on studies of this species.

Prey selectivity within species

In addition to selecting between prey species, O. marina discriminates between individuals of the same species with different properties. For example, O. marina preferentially selects virus-infected over healthy E. huxleyi when presented together at equal densities [START_REF] Evans | Preferential grazing of Oxyrrhis marina on virusinfected Emiliania huxleyi[END_REF]. The underlying mechanisms behind this selection are not fully known.

However, prey parameters that vary between healthy and virus infected prey and hence potentially influence feeding selectivity include prey cell size, prey cell surface properties, the release of dissolved infochemicals, and dimethylsulphoniopropionate (DMSP) lyase activity [START_REF] Brussaard | Flow cytometric analysis of phytoplankton variability following viral infection[END_REF][START_REF] Evans | Viral infection of Emilliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species[END_REF][START_REF] Evans | The relative significance of viral lysis and microzooplankton grazing as pathways of dimethlysulfoniopropionate (DMSP) cleavage: an Emiliania huxleyi culture study[END_REF][START_REF] Evans | Preferential grazing of Oxyrrhis marina on virusinfected Emiliania huxleyi[END_REF]. Other studies have investigated the ability of O. marina to discriminate between E. huxleyi strains with different DMSP lyase activity [START_REF] Wolfe | Grazing-activated chemical defence in a unicellular marine alga[END_REF]Strom et al., 2003a).

For example, [START_REF] Wolfe | Grazing-activated chemical defence in a unicellular marine alga[END_REF] found that although O. marina could tolerate high DMSP lyase-activity E. huxleyi strains, it avoided them when presented with both low and high activity strains [START_REF] Wolfe | Grazing-activated chemical defence in a unicellular marine alga[END_REF]. The enzyme DMSP-lyase cleaves DMSP to yield dimethyl sulphide (DMS) and acrylate, with the latter having potent antimicrobial activities [START_REF] Sieburth | Acrylic acid and "antibiotic" principle in Phaeocystis blooms in Antarctic waters[END_REF], and this potentially induces prey rejection. For a detailed review on the chemoreception associated with both of these examples of E. huxleyi intra-prey selectivity, the reader is directed to Breckels et al. (this issue).

Another well documented example of intra-species prey preference involves I. galbana as prey. When O. marina is grown in dense cultures of I. galbana, grazing ceases as prey become nitrogen limited, although grazing continues if the prey carbon:nitrogen ratio remains low [START_REF] Flynn | Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina. II. Release of nonprotein amines and feces during predation of Isochrysis[END_REF][START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF]. These results have been applied, to test various mechanistic mathematical model formulations that use prey carbon:nitrogen ratio as an index for prey quality (Davidson et al., 1995b;[START_REF] Mitra | The influence of changes in predation rates on marine microbial predator/prey interactions: a modelling study[END_REF][START_REF] Mitra | Predator-prey interactions: is "ecological stoichiomtry" sufficient when good food does bad?[END_REF] and the application of the models are further discussed by Davidson et al. (this issue). It has been suggested that this rejection of nitrogen deplete I. galbana by O. marina may be due to the build up of an inhibitor within predator cells or a change in prey recognition by the predator [START_REF] Flynn | Prey selection and rejection by a microflagellate; Implications for the study and operation of microbial food webs[END_REF][START_REF] Martel | Conceptual bases for prey biorecognition and feeding selectivity in the microplankton marine phagotroph Oxyrrhis marina[END_REF]. Without further experimental evidence, however, these suggestions remain speculative.

Although investigating prey preference within species is a promising approach to assess factors affecting prey selectivity, as it enables better control of certain prey variables, the main factors driving selection remain poorly understood. Clearly, we need to recognise how prey parameters including size, motility, cell surface properties, and dissolved chemical cues vary between and within different prey species. It is also essential to have a detailed understanding of the feeding mechanisms used by O. marina to search, capture, and ingest their prey (see [START_REF] Montagnes | Selective feeding behaviour of key free-living protists: avenues for continued study[END_REF].

'HOW' OXYRRHIS MARINA FEEDS

In common with other naked dinoflagellates, including Gyrodinium spirale and Noctiluca scintillans, O. marina feeds by direct engulfment, completely ingesting prey through a nonpermanent cytostome [START_REF] Elbrächter | Food uptake mechanisms in phagotrophic dinoflagellates and classification: a discussion[END_REF][START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF], consisting of a subsurface "microtubular basket" (Gaines and [START_REF] Gains | Heterotrophic Nutrition[END_REF]. To assess feeding mechanisms used by O. marina we will consider the individual feeding stages employed by this species: i.e. searching, contact, capture, processing, and ingestion (see Montagnes et al. 2008 for a synopsis of protist feeding stages, and note that digestion will not be covered within our work, which focuses on feeding per se). In particular, we highlight, as a priority for future study, the feeding stages that are least understood (Fig. 2).

Searching

Prey searching by motile protists is influenced by swimming speed and changes in direction and frequency of turning [START_REF] Montagnes | Selective feeding behaviour of key free-living protists: avenues for continued study[END_REF]. For a detailed assessment of swimming behaviour in O. marina, including discussion on helical paths in a three-dimensional environment, see Boakes et al. (this issue). In brief, O. marina swims in a helix, with an increase in the helical path as prey concentrations decrease [START_REF] Bartumeus | Helical Levy walks: adjusting searching statistics to resource availability in microzooplankton[END_REF]. Similar patterns are observed for other protists, such as some ciliates (e.g. [START_REF] Fenchel | The functional biology of Strombidium sulcatum, a marine oligotrich ciliate (Cilophora, Oligotrichina)[END_REF]. Changes in the helical motion are controlled by flagellar movement, and when prey concentrations are high (~10 4 -10 5 cells ml -1 ), O. marina invests more energy in using the longitudinal flagellum relative to the transverse flagellum, resulting in a helical path that is nearly linear, due to the low amplitude and frequency of gyres [START_REF] Bartumeus | Helical Levy walks: adjusting searching statistics to resource availability in microzooplankton[END_REF]. In contrast, at medium to low prey concentrations (~10 1 -10 3 cells ml -1 ), O. marina invests more energy in movement using the transverse flagellum, which results in an increase in the helical trajectories [START_REF] Bartumeus | Helical Levy walks: adjusting searching statistics to resource availability in microzooplankton[END_REF]. [START_REF] Bartumeus | Helical Levy walks: adjusting searching statistics to resource availability in microzooplankton[END_REF] suggested that these "helical walks" optimize random searching in three-dimensional environments with low prey densities.

Although changes in O. marina swimming behaviour are well documented, we lack an understanding of the mechanisms underpinning these changes (Boakes et al., this issue; Breckels et al., this issue). However, there is now strong evidence that O. marina exhibits a positive motile response towards chemical cues released by their prey. Furthermore, prey exudates and specific infochemicals (including certain amino acids and DMSP) can act as chemical cues [START_REF] Martel | Prey location, recognition. and ingestion by the phagotrophic marine dinoflagellate Oxyrrhis marina[END_REF][START_REF] Menden-Deuer | Individual foraging behaviors and population distributions of a planktonic predator aggregating to phytoplankton thin layers[END_REF]Breckels et al., this issue). The motile response of protists to chemical cues is often initiated by the binding of a dissolved chemoattractant molecule to a specific cell surface receptor [START_REF] Bell | Genetic dissection of attractant-induced conductances in Paramecium[END_REF][START_REF] Bagorda | Eukaryotic chemotaxis at a glance[END_REF]. Specifically, in O. marina, receptors involved in the motile response towards chemoattractants have not been identified, although a study involving cell signalling inhibitors has provided preliminary evidence that G-proteins, G-protein coupled receptors (GPCR), and protein kinases may be involved in the signalling pathways initiating motile behaviour [START_REF] Hartz | Using inhibitors to investigate the involvement of cell signaling in predation by marine phagotrophic protists[END_REF]. As highlighted in Breckels et al. (this issue), there is still much to learn about the involvement of dissolved chemoattractants in prey searching. In addition to dissolved chemical cues, light also appears to be an important environmental stimulus used in prey searching. O. marina exhibits positive phototaxis [START_REF] Droop | A note on the isolation of small marine algae and flagellates for pure cultures[END_REF][START_REF] Hartz | Investigating the ecological role of cell signaling in free-living marine heterotrophic protists[END_REF] and a pronounced diel cycle, with increased feeding and growth rates during the day [START_REF] Jakobsen | Circadian cycles in growth and feeding rates of heterotrophic protist plankton[END_REF]. This species possesses a number of rhodopsins [START_REF] Zhang | Spliced leader RNA trans-splicing in dinoflagellates[END_REF] and inhibition of these receptors significantly decreases its phototactic response [START_REF] Hartz | Investigating the ecological role of cell signaling in free-living marine heterotrophic protists[END_REF]. Preliminary experimental evidence indicates that O. marina may use rhodopsins to detect algal prey based on chlorophyll a autofluorescence [START_REF] Hartz | Investigating the ecological role of cell signaling in free-living marine heterotrophic protists[END_REF].

Contact, capture, and processing

Studying the feeding behaviour of O. marina remains challenging due to its relatively rapid swimming speeds (up to 700 µm s -1 ) and engulfment (<15 s) of prey [START_REF] Cosson | Swimming behavior of the unicellular biflagellate Oxyrrhis marina -In vivo and in vitro movement of the two flagella[END_REF][START_REF] Öpik | The digestive process of the dinoflagellate, Oxyrrhis marina Dujardin, feeding on the chlorophyte, Dunaliella primolecta Butcher -a combined study of ultrastructure and free amino-acids[END_REF]. Consequently, despite O. marina being a popular model predator, used extensively in feeding studies, we lack detailed understanding of the mechanisms used to contact, capture, and process prey by this dinoflagellate.

For bacterial prey, O. marina uses mainly the transverse flagellum to generate feeding currents that carry bacteria towards its cingular depression (Fig. 3). Within the cingular depression the bacteria are then carried in a spiral or linear path prior to being engulfed [START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF]. Thus, [START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF] considered O. marina to be an intercept feeder of bacteria, in that it produces a feeding current and directly intercepts food particles.

In contrast, when protists are prey, O. marina is raptorial, actively searching for prey [START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF]. In these cases, it swims at high speeds in narrow circles around the prey [START_REF] Barker | The culture and physiology of marine dinoflagellates[END_REF][START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF][START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF], and initial contact is made by the cell apex, the longitudinal flagellum [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF], or the transverse flagellum (Dodge andCrawford, 1971, 1974). Reports on the initial contact of the predator and prey are not consistent, with contact being noted both prior to [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF] and following [START_REF] Barker | The culture and physiology of marine dinoflagellates[END_REF][START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] the encircling of prey.

There are also contradictions regarding the use of trichocysts in prey capture (Fig. 2,3).

Although their presence, distribution, and ultrastructure in O. marina have been appreciated for some time [START_REF] Dradesco | Le flagellé Oxyrrhis marina. Cytologie, trichocystes position systématique[END_REF][START_REF] Dradesco | Sur la présence de trichocyst fibreux chez les Péridiniens; leur homologie avec les trichocysts fusiformes des Ciliés[END_REF][START_REF] Hausmann | Cytological studies on trichocysts. 6. Fine structure and mode of function of trichocysts in flagellate Oxyrrhis marina and ciliate Pleuronema marinum[END_REF][START_REF] Clarke | Occurrence of body scales in Oxyrrhis marina Dujardin[END_REF], we still lack detailed knowledge of their function in this species. Oxyrrhis marina appears to attach to its prey [START_REF] Öpik | The digestive process of the dinoflagellate, Oxyrrhis marina Dujardin, feeding on the chlorophyte, Dunaliella primolecta Butcher -a combined study of ultrastructure and free amino-acids[END_REF] and catch prey >3 µm using trichocysts [START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF] and may use filament-assisted prey capture [START_REF] Jacobson | Thecate heterotrophic dinoflagellates -Feeding behaviour and mechanisms[END_REF][START_REF] Goldman | Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina[END_REF]. Serial section analysis (by TEM), however, has failed to indicate discharged trichocysts during the early stages of phagocytosis, suggesting that they are not involved in prey capture [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF]. Despite the well documented involvement of trichocysts and filaments in prey capture by other alveolate species (e.g. [START_REF] Jacobson | Thecate heterotrophic dinoflagellates -Feeding behaviour and mechanisms[END_REF][START_REF] Hansen | Phagotrophic mechanisms and prey selection in freeliving dinoflagellates[END_REF][START_REF] Jeong | The ecological roles of heterotrophic dinoflagellates in marine planktonic community[END_REF][START_REF] Jakobsen | Hydromechanical signalling between the ciliate Mesodinium pulex and motile protist prey[END_REF], their function in O. marina evidently requires further elucidation.

Following prey capture, O. marina may reject certain food types during the prey processing stage [START_REF] Flynn | Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina. II. Release of nonprotein amines and feces during predation of Isochrysis[END_REF]Wolf et al., 1997). Prey types observed to have been rejected include nitrogen deplete I. galbana and E. huxleyi strains with high-activity DMSP lyase [START_REF] Flynn | Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina. II. Release of nonprotein amines and feces during predation of Isochrysis[END_REF]Wolf et al., 1997). Again, the mechanisms underlying this process are unknown.

Ingestion

Following contact, capture, and processing, prey are ingested by phagocytosis. For this to occur, the predator must first adhere to the prey [START_REF] Bozzaro | Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages[END_REF][START_REF] Cosson | Eat, kill or die: when amoeba meets bacteria[END_REF]. In other phagocytic cells, adherence commonly involves receptors on the phagocytic cell binding to specific ligands on the cell surface of their prey [START_REF] Ofek | Nonopsonic phagocytosis of microorganisms[END_REF] [START_REF] Stahl | The mannose receptor is a pattern recognition receptor involved in host defense[END_REF][START_REF] Bozzaro | Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages[END_REF]. Lectins, carbohydrate binding-proteins that agglutinate cells, commonly function as phagocytic receptors [START_REF] Venkataraman | Identification of a Gal/GalNAc lectin in the protozoan Hartmannella vermiformis as a potential receptor for attachment and invasion by the Legionnaires' disease bacterium[END_REF][START_REF] Lis | Lectins: carbohydrate-specific proteins that mediate cellular recognition[END_REF][START_REF] Stahl | The mannose receptor is a pattern recognition receptor involved in host defense[END_REF][START_REF] Roberts | Cell surface lectin-binding glycoconjugates on marine planktonic protists[END_REF]. Experimental evidence indicates the potential involvement of a mannose-binding lectin in prey adhesion and recognition by O. marina [START_REF] Wootton | Biochemical prey recognition by planktonic protozoa[END_REF]. However, it is unlikely that this is the only receptor involved in phagocytosis, as microbial recognition by phagocytic cells often involves numerous interacting receptors (Cambi and Figdor, 2005;Cambi et al., 2005).

Oxyrrhis marina appears to possess multiple cell membrane prey-binding proteins (Roberts, unpublished data); however, further characterisation and functional work is required to determine their role in feeding. Once the prey has bound to the cell surface of O. marina, phagocytosis is initiated through signal transduction pathways. Using cell signalling inhibitors, [START_REF] Hartz | Using inhibitors to investigate the involvement of cell signaling in predation by marine phagotrophic protists[END_REF] provided initial evidence that protein kinase signalling pathways may be involved in phagocytosis.

In O. marina, phagocytosis takes place at the non-permanent cytostome, which is located at the right ventral surface of the cell between the groove of the longitudinal flagellum and the ventral ridge microtubules (Fig. 3; [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF]. It involves the rearrangement of the microtubular cytoskeleton, an aspect of particular interest in dinoflagellates that feed by direct engulfment of large prey [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF][START_REF] Hansen | Phagotrophic mechanisms and prey selection in freeliving dinoflagellates[END_REF]. During phagocytosis, the anterior microtubular bands near the ventral surface of the cell are 'lifted' towards the ventral ridge microtubules [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF]. This reversible rearrangement of the cytoskeleton enables uptake of a wide size-spectrum of prey (see Types of prey, above). Following engulfment, the microtubular bands relocate to their original position within minutes. This organization of the microtubular cytoskeleton, forming two opposite focal points, has provided dinoflagellates with the flexibility required to evolve numerous feeding types, including the ability to directly engulf large prey particles [START_REF] Höhfeld | Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (dinophyceae) and its rearrangement during phagocytosis[END_REF]. Thus, although O. marina is not necessarily a typical dinoflagellate (Lowe et al., this issue-a), it may act as a model for certain aspects of dinoflagellate feeding.

THE CHALLENGE IN PERSPECTIVE: LINKING FEEDING BEHAVIOUR WITH

MECHANISMS

Although we have an in depth understanding of the type of prey that O. marina ingests, and the factors that affect grazing, knowledge of the underlying feeding mechanisms is incomplete and failure to understand these mechanisms may impinge on our ability to use it as a model species, in a wider context. For instance, there are still large gaps in our knowledge regarding the use of trichocysts in prey capture and the types of receptors employed to detect dissolved and cell surface prey cues. Gaining a more comprehensive understanding of the mechanisms underlying feeding behaviour in O. marina will be challenging, and if findings from laboratory-based experiments are to be applied to natural planktonic assemblages as a whole, careful consideration must be given as to whether this species is an appropriate environmental model. High swimming speeds in O. marina make swimming behaviour difficult to observe. However, rapid swimming is characteristic of many planktonic species (see [START_REF] Jeong | The feeding by the thecate mixotrophic dinoflagellate Fragilidium c.f. mexicanum on red tide and toxic dinoflagellate[END_REF][START_REF] Jeong | Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum[END_REF], suggesting that, although difficult, this is an appropriate avenue of research to pursue (see Boakes et al., this issue). From a molecular perspective, feeding mechanisms used by O. marina are poorly understood relative to other model protists, in particular Dictyostelium discoidium. In contrast to O. marina, D. discoidium receptors involved in chemotaxis and phagocytosis have been well characterized [START_REF] Cornillon | An adhesion molecule in free-living Dictyostelium amoebae with integrin beta features[END_REF][START_REF] Bagorda | Eukaryotic chemotaxis at a glance[END_REF]. Also, the complete genome of O. marina

has not yet been sequenced and given the immense genomes typical of dinoflagellates [START_REF] Hackett | Insight into a dinoflagellate genome through expressed sequence tag analysis[END_REF], potentially including O. marina [START_REF] Sano | Localization and copy number of the protein-coding genes actin, α-tubulin, and HSP90 in the nucleus of a primitive dinoflagellate, Oxyrrhis marina[END_REF], this remains a significant challenge that deserves pursuing (see Slamovits and Keeling, this issue). In addition, methods for generating large libraries of mutants, an approach used extensively with D. discoidium [START_REF] Annesley | Dictyostelium discoideum-a model for many reasons[END_REF]; http://dictybase.org), are currently unavailable for O. marina, although the many strains now available (see Lowe et al., this issue-a; Watts et al., this issue) may provide a valuable resource to this end. In contrast to other marine protist predators, however, the ease of maintaining O. marina in axenic and monoxenic culture (Lowe et al., this issue-b) provides an advantage for developing molecular approaches that can then be applied to a broader range of environmentally relevant species. Thus, we see great potential for the continued use of O. marina in this context. Interpreting how underlying mechanisms drive feeding efficiency and selectivity in planktonic protists is a challenging task. Currently, however, for many protist species we only have a limited knowledge of feeding mechanisms, and consequently lack fundamental information regarding how protist predators recognise prey and feed. As a result we experience difficulties in interpreting isolated laboratory feeding experiments and applying the findings to natural assemblages as a whole. Although care must be taken when generalizing from one protist predator to another, we recommend O. marina as a model predator to investigate and build a thorough understanding of feeding mechanisms, providing a methodological framework that can then be applied to other environmentally relevant protists. We consider that pursuing this approach would enable increased understanding of the functional elements that play such a fundamental role in driving and structuring aquatic microbial foodwebs. Amphidinium carterae [START_REF] Jeong | Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp[END_REF]; Heterosigma akashiwo [START_REF] Jeong | Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers[END_REF]; Cafeteria sp. (Jeong et al., 2007b); Pfiesteria piscicida, Stoeckeria algicida, Luciella masanensis, (Jeong et al., 2007a); mixed natural bacteria [START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF]; Dunaliella primolecta, Chlamydomonas spreta, Brachiomonas submarina, Nanochloropsis oculata [START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF]; Isochrysis galbana [START_REF] Kimmance | Do temperature-food interactions matter? Responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina[END_REF]; Dunaliella primolecta*, Dunaliella primolecta** (unpublished data, Yang and Montagnes, using two strains of O. marina as predators,*351_FAR01, **45_BOG01, Univ. Liverpool cultures of O. marina).

Note, responses derived for O. marina with Dunaliella primolecta*, Dunaliella primolecta** were performed on predator cultures that had been acclimated to prey levels for several days, which may explain the different shape of the responses, compared to other studies that tend to not acclimate or acclimate for a relatively short period. Note also that all responses, except those by [START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] follow Eq. 1 (see text); [START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] included a threshold prey level, where feeding stops and Eq. 1 is modified as I = I max ×(p-T)/(k+p-T), where T is the threshold level (ng C ml -1 ). Responses are for Amphidinium carterae [START_REF] Jeong | Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp[END_REF]; Heterosigma akashiwo [START_REF] Jeong | Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers[END_REF]; Cafeteria sp. (Jeong et al., 2007b); Pfiesteria piscicida, Stoeckeria algicida, Luciella masanensis, (Jeong et al., 2007a); mixed natural bacteria [START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF]; Dunaliella primolecta, Chlamydomonas spreta, Brachiomonas submarina, Nanochloropsis oculata [START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF]; Isochrysis galbana [START_REF] Kimmance | Do temperature-food interactions matter? Responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina[END_REF]; Dunaliella primolecta*, Dunaliella primolecta** (unpublished data, Yang and Montagnes, using two strains of O. marina as predators,*351_FAR01, **45_BOG01, Univ. Liverpool cultures of O. marina). Note, responses derived for O. marina with Dunaliella primolecta*, Dunaliella primolecta** were performed on predator cultures that had been acclimated to prey levels for several days, which may explain the different shape of the responses, compared to other studies that tend to not acclimate or acclimate for a relatively short period. Note also that all responses, except those by [START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] follow Eq. 1 (see text); [START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] included a threshold prey level, where feeding stops and Eq. 1 is modified as I = Imax(p-T)/(k+p-T), where T is the threshold level (ng C ml-1). 150x96mm (300 x 300 DPI)

  measured changes in abundance and biovolumes of O. marina and the prey D. primolecta, I. galbana, and M. pusilla over 22 d, starting with low initial predator and prey concentrations. They assessed selective grazing on the basis of 'equivalent encounter distance', which is the distance an average sized predator would have to swim to encounter a

  Past experiments have tended to involve bulk additions of potential chemoattractants and fail to simulate actual chemical gradients that occur around the prey. Given the tractability of culturing and observing O. marina, it should provide a good model for investigating the response of protist predators to chemical gradients that occur around the vicinity of prey cells.

Fig. 1 .

 1 FIGURE LEGENDS

Fig. 2 .

 2 Fig.2. Linking protist feeding steps with Oxyrrhis marina specific feeding mechanisms and

Fig. 3 .

 3 Fig. 3. Oxyrrhis marina with ingested prey. A-C Sections through O. marina containing

Fig. 1 .

 1 Fig.1. A comparison of functional responses of Oxyrrhis marina feeding on different prey, over a range of prey biomass, all conducted at either 20 or 21 ºC. Responses are for Amphidinium carterae[START_REF] Jeong | Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp[END_REF]; Heterosigma akashiwo[START_REF] Jeong | Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers[END_REF]; Cafeteria sp.(Jeong et al., 2007b); Pfiesteria piscicida, Stoeckeria algicida, Luciella masanensis,(Jeong et al., 2007a); mixed natural bacteria[START_REF] Jeong | Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria[END_REF]; Dunaliella primolecta, Chlamydomonas spreta, Brachiomonas submarina, Nanochloropsis oculata[START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF]; Isochrysis galbana[START_REF] Kimmance | Do temperature-food interactions matter? Responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina[END_REF]; Dunaliella primolecta*, Dunaliella primolecta** (unpublished data, Yang and Montagnes, using two strains of O. marina as predators,*351_FAR01, **45_BOG01, Univ. Liverpool cultures of O. marina). Note, responses derived for O. marina with Dunaliella primolecta*, Dunaliella primolecta** were performed on predator cultures that had been acclimated to prey levels for several days, which may explain the different shape of the responses, compared to other studies that tend to not acclimate or acclimate for a relatively short period. Note also that all responses, except those by[START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] follow Eq. 1 (see text);[START_REF] Fuller | The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina[END_REF] included a threshold prey level, where feeding stops and Eq. 1 is modified as I = Imax(p-T)/(k+p-T), where T is the threshold level (ng C ml-1). 150x96mm (300 x 300 DPI)

Fig. 2 .Fig. 3 .

 23 Fig.2. Linking protist feeding steps with Oxyrrhis marina specific feeding mechanisms and influential prey parameters. 162x219mm (300 x 300 DPI)

Table 1 .

 1 Parameters for the functional responses depicted in Fig.1. See Fig.1legend for an explanation of the parameters and sources of the data.

	I max (ng C d -1 ) T (ng C ml -1 ) k (ng C ml -1 )	Prey
	1.25		704	Heterosigma akashiwo
	2.80		90	Amphidinium carterae
	0.29		455	Cafeteria sp.
	0.33		83	Pfiesteria piscicida
	0.14		89	Stoeckeria algicida
	0.07		132	Luciella masanensis
	0.07		44	Bacteria
	1.10	19.5	127	Dunaliella primolecta
	1.97	12.4	388	Chlamydomonas spreta
	1.29	41.8	146	Brachiomonas submarina
	1.37	-0.77	182	Nanochloropsis oculata
	1.43		781	Isochrysis galbana
	1.22		4538	Dunaliella primolecta*
	2.30		19300	Dunaliella primolecta **

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ACKNOWLEDGEMENTS

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Journal of Plankton Research

The Authors would like to thank Michael Steinke and Mark Breckels for their constructive comments on this manuscript. We would also like to thank the Associate Editor and the anonymous reviewers for their helpful suggestions.

FUNDING

This work was, in part, supported by: UK NERC grants NE/C519438/1 and NE/G010374/1 awarded to ECR and E. Dudley, and NE/F005237/1 awarded to P. C. Watts, CDL, and DJSM; the Ecological Disturbance Research Program of Korea Institute of Marine Science and Technology Promotion/Ministry of Land, Transportation and Marine Affairs (KMLTM) awarded to HJJ; and the SAMS/NERC Oceans 2025 programme supporting KD.