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Home , Emiliania huxleyi, Micromonas, Oxyrrhis marina

AQUATIC MICROBIAL Vol. 10: 307-313,1996 Published June 27 Aquat Microb Ecol l

NOTE

Grazing in the heterotrophic marina: size selectivity and preference for calcified cells

Frank C. Hansen, Harry J. Witte*,Jutta Passarge"

NeUlerlands Institute for Sea Research. PO Box 59, 1790 AB Den Burg,The Netherlands

ABSTRACT: Selective on nanophythoplankton by the to as large as 0. manna itself, like Cricosphaera heterotrophic dinoflagellate Oxyrrhis manna was investi- elongata (20 to 30 pm) (see Droop 1966). On the other gated in laboratory expenments. 0. marina was offered 2 hand, marina also seems to be able to discriminate mixtures of differently sized algae: (1) pusiUa 0. (2 pm Equivalent Spherical Diameter), Emihania huxleyi between food (Tarran 1992). The experiments (5 pm ESD), and Tetraselrms sueclca (7 pm ESD); and (2)Nan- presented here were designed to test (1) size-selectiv- nochloris sp. (2 pm ESD), (5 pm ESD), ity in 0. marina grazing and (2) whether or not E. hux- sp. (8 pm ESD). and Tetraselmis sp. (10 pm leyi may form an exception within its size class. In con- ESD). 0. marina grazed selectively on the larger algal species trast to most previous dinoflagellate grazing studies, (ESD 2 7 pm), and also selected for the larger cells within each species. 0. marina discriminated against E. huxleyi. To test we used mixtures of food items. this selection, 0. marina was offered mixtures of equal con- Material and methods. and the centrations of the similarly sized algae E. huxleyj and I. gal- algal species were obtained from the NIOZ culture col- band. In these mixtures, 0. marina preferred the calcified E. lection (Netherlands Institute for Sea Research, Dept huxleyl cells over noncalcified E. huxleyj cells and discrimi- nated against I. galbana. This result is also interpreted in Biological Oceanography). They were grown semi- terms of size-selective grazing. continuously in batch cultures in autoclaved f/2- medium (Guillard & Ryther 1962) at 15OC and illumi- KEYWORDS: . Food selection - Prey size . Micro- nated 16 h light:8 h dark with 60 pE m-2 S-'. 0.marina . was fed Isochrysis galbana and Rhodomonas sp. In 3 incubation expenments Oxyrrhis marina (18 pm Equivalent Spherical Diameter, ESD) was offered dif- Heterotrophic are now recognized ferent mixtures of algal species (Table 1). The experi- as a ubiquitous, important component of the pelagic ments were performed in 600 m1 glass bottles mounted protozoan comn~unity that feeds on pico- and nano- on a rotating device (0.5 rpm), kept at 15°C and illumi- phytoplankton (Lessard 1991). Size-selective grazing nated with 10 pE m-2 S-' light (16:8 h). Prior to the in protozoans (Fenchel 1980, Jonsson 1986, Rassoul- experiments, 0. marina was pre-adapted for 24 h to all zadegan et al. 1988) has been examined; however, experimental conditions, including food composition little is known about the food preferences of hetero- and concentrations. The algae used to restore the ini- trophic dinoflagellates (Hansen 1992). tial concentrations after the adaptation period, were The widespread species Oxyrrhis marina was used also adapted to the low light conditions. as a to study selective grazing in an In the experimental and control bottles (i.e. with and omnivorous phagotrophic dinoflagellate. 0. marina, without Oxyrrhis marina), cell concentrations and cell which can reach high abundances in rockpools and sizes of all species were followed for 48 h. Measure- salt lakes, has also been found in the White Sea, the ments of 0. marina (Expts 1, 2, and 3) and algal con- western Baltic, the English Channel and in the Medi- centration and size distribution (except Micromonas terranean Sea (Kofoid & Swezy 1921). This species has pusilla) in Expt 1 were made on unpreserved samples been reported to feed on a wide range of particle sizes, using a 128-channel electronic particle counter (Parti- from small algae like Nannochloris oculata (2 to 4 p) cle Data Inc.). Algae in Expts 2 and 3 were measured without preservation applying flow cytometry (Coulter 'Addressee for correspondence. E-mail: [email protected] Epics XL) on the basis of their fluorescence character- "Present address: Dept of Microbiology, University of Ams- istics (Fig. la, b). Calcified Emiliania huxleyi cells were terdam, 1018 VS Amsterdam, The Netherlands distinguished from noncalcified cells by their side-

0 Inter-Research 1996 308 Aquat Microb Ecol 10: 307-313,1996

Table 1. Experimental set-up with initial Oxyrrhis marina bio- respectively. Grazing rates were calculated from con- volume concentrations and ~nltialcell sizes and b~ovolumes centration changes of all species, including 0. manna, of the food algae. n: number of replicates, ESD: equivalent in the experimental bottles compared to the controls spherical diameter following Frost (1972). Electivity-indices (a)were cal- culated from clearance rates and statistically tested, as Oxyrrhis Food algae Size Cell described by Chesson (1983) for selection experiments marina (species) (ESD, volume (pm3 ml-l) pm) (pm3) with changing food densities. For display purposes, the a were transformed to E, with -1 2 e 5 +l, following Expt 1 2.2 X 106 M~crornonaspusilla 1.6 2 Chesson (1983). (n= 1) Emiliania huxleyi 5.2 73 Results. Due to the chosen Light conditions, algal 7.0 183 biovolume changes in the controls were insignificant Expt 2 16.6 X 106 Nannochloris sp. 1.7 2 (Figs. 2a, c & 3a); therefore, rates of changes in the ex- (n = 4) Isochrysis galbana 5.0 64 perimental bottles containing Oxyrrhis marina reflect Rhodomonas sp. 7.8 250 Tetraselmis sp. 9.8 492 grazing rates, which are listed in Table 2. In the experi- mental bottles, biovolume concentrations significantly Expt 3 12.3 X 106 Emiliania huxleyi 4.7 declined in the larger sized algae Tetraselmis suecica, (n = 4) Isochrysis galbana 4.7 Rhodomonas sp. and Tetraselrnis sp. Within Expts 1 and 2, 0. marina grazed on these larger algae with higher clearance rates than on the smaller algae (Table 2). scattering properties (flow cytometry, see Fig. lc). Due to the much lower algal and higher Oxyrrhis Inverted rnicroscopy was used to count preserved (2 % marina concentrations used in Expt 2, rates of biovol- acid Lugol's solution) samples of M. pusilla and to ume changes were higher than in Expt 1. In Expt 1, additionally control for the fraction of calcified E. hux- large cells remained through the 48 h of the experi- leyi (1 % glutaraldehyde). ment (Fig. 2b), whereas in Expt 2 they were almost Cell volumes of algae and Oxyrrhis marina were cor- totally removed within the first 6 h (Fig. 2d). Despite rected by species-specific comparison with live cell higher maximum clearance rates, the ingestion rates volumes measured with an Image-Analysis-System and biovolume-specific daily rations of 0.manna were (Leica Quantimet 570) at 500x or 125x magnification, higher in the Expt 1 (Table 2), in which food density

.-B 10000 c Fig. Simultaneous mea- 2 1. - a,.,.,. surement of different algal specles by flow cyto- L 0 1 / , , ] metry. (a) Expt 2. N: Nan- 100 nochloris sp.; I: Isochrysis =Q),, 1 galbana; R: Rhodomonas g': I0 sp.; T. Tetraselmis sp. m m b2 (b) Expt 3. (c) Expt 3. Cal- cified and noncalcified 10 100 100010000 m l i 10 100 1000 IOOOO 1 10 100 1000 IOOOO Emiliania huxleyi cells chlor. fluor. [rel. units log scale] size [rel. unib log scale] size [rel. units log scale]

l 10 100 1000 chlor, fluor. [rel. units log scale] size [rel. units log scale] size [rel. units log scale] Hansen et al.:Grazing in Oxyrrhis marina 309

time [h] time [h] (c) (d

Rhodornonas

Isochrysis Nannochloris

0 6 12 18 24 30 36 42 48 0 6 12 18 24 30 36 42 48 time [h] time [h] Fig. 2. Mean algal biovolume concentrations over 48 h in incubations without (a, c; controls) and with (b, d) Oxyrrhis marina. (a, b) Expt 1: Micromonaspusilla (2 pm), Emiliania huxleyi (5 ).]m)and Tetraselmis suecica (7 pm) (c, d) Expt 2: Nannochloris sp. (2 pm) Isochrysis galbana (5 pm),Rhodomonas sp. (8 pm) and Tetraselmis sp. (10 pm). Note: there were 2 Tetrasehis species which were different in size (different shading) was much higher. In both experiments, the moderately Positive selection of the larger cells is explicitly sized algae (Erniliania huxleyi and Isochrysis galbana, demonstrated by the Chesson-indices (Fig. 4a ,b). As respectively) declined at a slower rate than did the long as they were available at concentrations 220 cells larger algae, and concentrations changed least in the ml-', the large Rhodomonas and Tetraselmis species smallest algae, Micrornonas pusilla and Nannochloris were consumed in preference to the smaller algae. At sp. (Fig. 2b, d). even lower concentrations of these algae, Rhodornonas

Emilianfa Isochrysis

0 6 12 18 24 30 36 42 48 0 6 12 18 24 30 36 42 48 time [h] time [h] l Fig. 3. Expt 3. Mean biovolume concentrations of Emiliania huxleyi and Isochrysis galbana over 48 h incubations without (a; control) and with (b) Oxyrrhis marina 310 Aquat Microb Ecol 10: 307-313. 1996

Table 2. Mean algal concentrations (X 1000 pm3 rnl-l),volume-specific clearance rates [X 1000 pm3 (pm30xyrrhis)-' d-'1, inges- t~onrates (cells Oxyrrhi~'d-l) and volume-specific daily rations (% d-l) for Oxyrrhis marina feeding on 7 different algal species during 3 incubation experiments

Expt Time Food algae (species) Algal conc. Clearance rate Ingestion SDR no. Mean SE Mean SE rate (% d-l)

00-12 h lMicromonas pusilla 719 - -45 - - 65 12-24 h ~Micromonaspusilla 617 - 7 6 96 24 -48 h Micromonas pusilla 449 - 54 5 1 00-12 h Emiliania huxleyi 9447 - -1 1 -6 12-24 h Emiliania huxleyi 9190 - 15 8 24 -48 h Emiliania huxleyi 7896 - 20 11 00-12 h Tetrasehis suecica 3283 - 560 40 12-24 h Tetraselmis suecica 2186 - 132 6 24-48 h Tetraselmis suecica 1296 - 174 6 00-06 h Nannochloris sp. 169 2 16 5 06-24 h Nannochloris sp. 132 5 40 10 24-48 h Nannochlons sp. 68 4 42 5 00-06 h Isochrysis galbana 94 9 3 142 10 06-24 h Isochrysis galbana 366 20 148 4 24-48 h Isochrysis galbana 30 6 209 0 00-06 h Rhodomonas sp. 126 2 1430 5 06-24 h Rhodomonas sp. 1.3 0.0 225 0 24-48h Rhodomonassp. 0.2 0.0 86 0 00-06h Tetraselmissp. 77 6 1196 1 06-24 h Tetraselmis sp. 6.1 0.5 -43 -0 24-48 h Tetraselmis sp. 5.4 0.7 -27 -0 00-02 h Emiliania huxleyi 1349 42 961 84 02-12 h Emiliania huxleyi 663 12 -21 - 1 12-48 h Emiliania huxleyi 359 7 6 1 1 00-02 h Isochrysis galbana 2185 16 87 11 02-12 h Isochrysis galbana 1685 11 101 10 12-48 h Isochrysis galbana 348 16 226 4

sp. was still positively selected, but grazing on Tetra- After 6 h, when the concentrations of the large algae selmis sp, ceased (Fig. 4b, Table 2). A multivariate test were diminished to very low levels, Oxyrrhis marina on the Chesson-indices of the first period of Expt 2, fed primarily on the moderately sized Isochrysis gal- when all algal species were sufficiently abundant, bana (Fig. 4b), which was grazed down during the rest showed the preference for the large algal species to be of the experiment in preference to the small Nan- significant (p < 0.05, Hotelling t-test). nochlons sp. (Figs. 2d & 4b). The (negative) Chesson-

time-interval of incubation time-interval of incubation

Fig. 4. Chesson-indices of Electivity (E) for Oxyrrhis marina simultaneously offered differentlysized algal species (see Fig. 2): -1 5 e t +l, with E < 0 indicating negative, E > 0 positive, and E = 0 no selective grazing. (a)Expt 1. (b)Expt 2. "Large SDdue to very low concentrations; mean i SD,n = 4 Hansen et al.: Grazing in Oxyrrhjs marina

fl I Nannochloris I

algae species

Fig. 7. Expts 2 and 3. Algal cell volume as % of cell volume in time-interval of incubation controls after 24 h grazing (for Rhodomonas sp. and Tetraselmis sp. after 12 h) by Oxyrrhis manna. Mean * SD, Fig. 5. Chesson-indices of Electivity (E)for Oxyrrhis manna n=4 simultaneously offered Enuhania huxleyl and Isochrysis gal- band -1 5 E 2 +l, with E < 0 indicating negative, & > 0 positive, and E = 0 no selective grazing. Mean * SD, n = 4 cant (Student's t-test, p < 0.05). While in the controls the percentage of calcified E. huxleyi cells remained indices of the smaller algae increased during the constantly high (92 * 2 %), the percentage in the exper- experiments, while the concentrations of the preferred, imental bottles declined sharply to 17 % (Fig. 6), indi- larger algae diminished. As a result, after 12 h the cating a strong selection for calcified over noncalcified smallest species, Micromonas pusilla, was consumed cells of E. huxleyi. almost in proportion to its abundance (E = 0, Fig. 4a). After 24 h grazing by Oxyrrhis marina, the mean cell However, considerable discrimination remained size in all algal species was significantly reduced (p against the moderately sized and most abundant alga 0.01, Student's t-test) in comparison to their sizes in the EmiLiania huxleyi (Fig. 4a) and the small Nannochlons controls (Fig. 7). This indicates a preference of 0. sp. (Fig. 4b). marina for larger cells within the species. In Expts 1 and 2, Emiliania huxleyi was the only In Expt 3 controls, a daily rhythm in Emiliania hux- moderately sized alga that was selected against. More leyi cell size was found. E. huxleyi showed synchro- proof of a special feeding behaviour of Oxyrrhis nized , with cell division at the end of the marina towards E, huxleyi was demonstrated in Expt 3, dark period (Fig. 8), which is in accordance with obser- where the similarly sized Isochrysis galbana and E. vations by van Bleijswijk et al. (1994).However, such a huxleyi were simultaneously offered. 0, marina did rhythm was missing in the bottles with grazing, indi- not select against E. huxleyi in the first hours of the cating that Oxyrrhis marina fed selectively on the experiment. However, thereafter, 0.marina preferred actively growing and dividing cells. I. galbana (Figs. 3 & 5). All preferences were signifi-

01.I.I.I.I.I.I.I.I~ 0 6 12 18 24 30 36 42 48 time [h] 0 6 12 18 24 30 36 42 48 tlrne [h] Fig. 6. Expt 3. Fraction of calcified Edania huxleyi cells (% total E. huxleyi cell concentration) over 48 h incubations with Fig. 8. Expt 3. Mean cell size in Emiliania huxleyi over 48 h (grazing) and without (control) Oxyrrhis marina. Mean * SD, incubations with (grazing) and without (control) Oxyrrtus n = 4. Where error bars are invisible, they fall within the size marina. Mean i SD,n = 4. Where error bars are invisible, they range of the symbols fall within the size range of the symbols 312 Aquat Microb Ec

Discussion. In Expts 1 and 2, initial concentrations of obviously, size is a major selection criterium in the different algal species were not equal and their Oxyrrhis manna. Size-selective grazing has also been proportions changed during the incubations. We shown for (Monger & Landry 1991, Hansen applied the Chesson-index, which is especially suited 1992), and (Fenchel 1980, Jonsson 1986, Ras- to measuring selectivity under these conditions. It soulzadegan et al. 1988). Ciliates were shown to have measures any deviation from random foraging inde- an optimum prey size and their size-selectivity has pendent of changes in food item concentrations, and been explained by the structure of their feeding appa- does not change unless the behaviour of the grazer ratus (e.g. Fenchel 1980). In many flagellates such changes (Chesson 1983). According to optimal forag- elaborate feeding structures are missing. The flagel- ing theory for a predator handling individual prey late 0.marina uses its tranverse to contact items, selective behaviour towards a less preferred and capture the prey particles (Dodge & Crawford prey (i)is not influenced by the abundance of i, but by 1971, 1974). This flagellum is equipped with hair-like the abundance of the energetically more optimal, pre- projections, which may have a function in particle ferred prey (Charnov 1976). If the larger algae were selection. Tarran (1992) observed differential feeding the preferred prey, they would remain preferred irre- by 0, marina on , but ascribed selectivity spective of the abundance of the smaller algae. Thus, rather to feeding history than to prey size. Therefore, the relatively low biomass of the smallest algal species 0. marina was pre-adapted to the food compositions should neither have influenced the selective behaviour used in the experiments of this study. Hansen (1992) of Oxyrrhis manna towards themselves, nor towards found size-selective grazing to occur in the dinoflagel- the preferred, larger algal species. late Gyrodinium spirale. G. spirale was shown to have The number of experiments and food species tested an optimum prey size, which is similar to its own size. was limited, and food quality related properties other The size-related preference of 0. marina for large par- than size, e.g. biochemical clues (smewtaste), shape or ticles (this study) is in accordance with the results for mobility, may differ between the species tested and G, spirale. Hotvever, in 0. marina, there was some may also have affected grazing selectivity. Chemosen- indication for, relative to the size of the grazer, a lower sory ability has been shown to exist in flagellates (Ben- optimum food size. nett et al. 1988). However, selection experiments with In the present multispecies study, grazing on Emilia- Oxyrrhis marina grazing on a microalgae (Dunaliella nia huxleyi occurred but, in most cases, a negative terticolata) and flavoured and unflavoured latex beads selection was found. The observed discrimination suggested that 0. marina is unable to distinguish par- against E. huxleyi in Expt 1 can not be explained by its ticles on the basis of smell or taste (Tarran 1992). Cell size, since E. huxleyi was intermediate In size to shapes were not very different in our experiments: Micromonas pusilla and Tetraselmis suecica. Perhaps ovoid in case of Rhodomonas sp. and both Tetraselmis deterrent substances played a role. Grazing on the species and globoid in all other species. It is doubtful microalga Phaeocystis cf. globosa by that 0. marina could differentiate between such small (Hansen & van Boekel 1991) and by protozoans, differences in shape. including Oxyrrhis marina (Hansen et al. 1993), was Grazing activity may be most directly documented also found to be very low, and DMSP (dimethylsulfo- by the clearance rate, which we expressed per unit niopropionate)-related substances have been sug- biovolume of the grazer to account for differences in gested to work as anti-grazing compounds (e.g. Estep grazer size. Compared to Expt 1, maximum clearance et al. 1990). Whether a possible release of DMSP- rates were 2 to 3 times higher in Expts 2 and 3, indicat- related substances by E. huxleyi played a role in our ing feeding saturation at the high initial food concen- experiments is not known and remains speculative. trations in the Expt 1 (Table 2). Maximum clearance An exception to the discrimination against Emiliania rates and specific daily rations found in the first periods huxleyi was the selection of the calcified over noncalci- of the experiments were in the same range as reported fied E. huxleyi and in preferrence to Isochrysis galbana in previous studies on Oxyrrhis marina (Tarran 1992 (Expt 2). Since calcified E. huxleyi are bigger than both and references therein), and would allow growth rates other cell types, 89 pm3 compared to 55 pm3 and up to 0.9 doublings d-' (with -50% gross growth effi- 57 pm3 (apparent ESD at t = 0 h),the preference for the ciency, Davidson et al. 1995).The specific daily rations calcified cells could be explained by size-selectivity. found during the remainder of Expts 2 and 3 were too The possession of coccoliths does not seem to be an low to support growth of 0. marina, which is in accor- effective defence mechanism, as has been suggested dance with the observed small changes in their bio- (Young 1994). On the contrary, coccoliths make the mass (not shown). cells larger and, in this study, more susceptible to graz- The selection for larger particles was consistently ing by Oxyxrrhis manna. Indeed, in experiments with found in all experimental treatments of this study and, E. huxleyi as the sole food or in bloom situations, graz- Hansen et al.. Grazing in Oxyrrhis marina 313

ing on E. huxleyi by microzooplankton (Holligan et al. pouchetii as a function of the physiological state of the 1993), including marina (Tarran & Burkill 1995), has prey. Mar Ecol Prog Ser 67:235-249 0, Fenchel T (1980).Relation between particle size selection and been shown. clearance In suspension-feeding ciliates. Lirnnol Oceanogr One reason why microzooplankton may have a sig- 25(4): 733-738 nificant impact on Emiliania huxleyi populations is the Frost BW (1972) Effects of size and concentration of food par- preference, at least by Oxyrrhis mar~na,for the grow- ticles on the feeding behaviour of the marine planktonic Calanus pacificus. Limnol Oceanogr 17:805-815 ing and dividing cells of E. huxleyi. If the grazers selec- Guillard RRL, Ryther JH (1962) Stud~esof marine planktonic tively remove the metabolically active fraction of an . I. Cyclotella nana Hustedt and Detonula confer- algal population, their impact would be much greater vacea Cleve. Can J Microbiol 8:229-239 than would be estimated from numerical cell losses. Hansen FC, Reckermann M. Klein Breteler WCM, Riegman R Hetero- and mixotrophic dinoflagellates form a sub- (1993) Phaeocystis blooming enhanced by copepod preda- tion on protozoa: evldence from Incubation experiments. stantial part of the herbivorous community. These Mar Ecol Prog Ser 102:51-57 organisms may show feeding behaviour like that Hansen FC, van Boekel WHM (1991) Grazing pressure of the observed for Oxyrrhis marina. However, it is clear that calanoid copepod Temora longicornis on a Phaeocystis more investigations on selective grazing in hetero- dominated in a Dutch tidal inlet. Mar Ecol Prog Ser 78:123-129 trophic dinoflagellates are needed. Hansen PJ (1992). . Prey size selection, feedins- rates and growth dynamics of heterotrophic dinoflagellates with svecial emphasis on Gvrodinium s~irale.Mar Biol 114: Acknowledgements. We thank Mrs Anna Noordeloos for pro- 3'27-334 viding us with algal stock cultures. Dr Wim Klein Breteler and Holligan PM, Fernandez E. Aiken J, Balch WM. Boyd P. Dr Marcel Veldhuis are thanked for assistance in image- Burkill PH. Finch M, Groom SB, Malin G, M,ller K, Purdie analysis and flow cytometry. Mr Jaap van der Meer is DA, Robertson C, Trees C, Turner SM, van der Wal P thanked for mathematical and statistical advice. Furthermore, (1993) A biogeochemical study of the we are indebted to Dr Wim Klein Breteler, Dr Roe1 Rlegman, Emiliania huxleyi in the North Atlantic. Global Biochem Dr Marcel Veldhuis and Dr Judith van Bleijswijk for their Cycles 7(4):879-900 valuable comments and Mr Paul Boudreau for linguistic Jonsson PR (1986) Particle size selection, feeding rates and improvements of the manuscript. growth dynamics of marine planktonic oligotrich ciliates. Mar Ecol Prog Ser 33:265-277 Kofoid CA, Swezy 0 (1921) The free-living unarmored LITERATURE CITED dinoflagellates. Memoires of the University of California 5. California Press, Berkeley Bennet SJ, Sanders RW, Porter KG (1988) Chemosensory Lessard EJ (1991) The trophic role of heterotrophic dinofla- responses of heterotrophic and mixotrophic flagellates to gellates in diverse marine environments. Mar Microb potential food sources. Bull Mar Sci 43:764-771 Food Webs 5:49-58 Charnov EL (1976) Optimal foraging: attack strategy of a Monger BC, Landry MR (1991) Prey-size dependency of graz- mantid. Am Nat 110:141-151 ing by free-living marine flagellates. Mar Ecol Prog Ser 74: Chesson J (1983) The estimation and analysis of preference 239-248 and its relationship to foraging models. Ecology 64(5): Rassoulzadegan F, Laval-Peuto M, Sheldon RW (1988) Parti- 1297-1304 tioning of the food ration of marine ciliates between pico- Davidson K, Cunningham A. Flynn KJ (1995). Predator-prey and nanoplankton. Hydrobiologia 159:75-88 interactions between Isochrysis galbana and Oxyrrhis Tarran GA (1992) Aspects of the grazing behaviour of the manna. 111. Mathematical modelling of predation and marine dinoflagellate Oxyrrhismarina Dujardin. PhD the- nutrient regeneration. J Kes 17(3):465-492 sis, University of Southampton Dodge JD, Crawford RM (1971) Fine structure of the dinofla- Tarran GA, Burkill PH (1995) Effects of temperature and con- gellate Oxyrrhis marina 11. The flagellar system. Protisto- centration on the mortality and transformation of Emilia- logica 7(4):399-409 nia huxleyi due to protozoan grazing. Conference on Ernil- Dodge JD, Crawford RM (1976) Fine structure of the dinofla- iania huxleyi and the oceanic carbon cycle, The Natural gellate Oxyrrhis marina 111. Phagotrophy. Protistologica History Museum, London, 5-8 Apnl 1995 (abstract vol- 10(2):239-244 ume) Droop MR (1966) The role of algae in the nutrition of Heter- Van Bleijswijk JDL, Kempers R, Veldhuis MJ (1994) Cell and amoeba clara Droop with notes on Oxyrrhis marina growth characteristics of types A and B of Emiliania hux- Dujardin and Phdodina roseola Ehrenberg. In: Barnes H leyi () as determined by flow cytometry (ed) Some contemporary studies in marine science. Allan and chermcal analysis. J Phycol 30:230-241 and Unwin, London, p 269-282 Young JR (1994) Function of coccoliths. In: Winter A, Siesser Estep KW, Nejstgaard J, Skjoldal HR, Rey F (1990) Predation WG (eds) . Cambridge Univ Press, Cam- by copepods upon natural populations of Phaeocystis bridge, p 63-82

Responsible Subject Editor: J. Dolan, ViLlefranche-sur-Mer, Manuscript first received: September 25,1995 France Revised version accepted: April 10, 1996