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Grazing in the Heterotrophic Dinoflagellate Oxyrrhis Marina: Size Selectivity and Preference for Calcified Emiliania Huxleyi Cells

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Grazing in the Heterotrophic Dinoflagellate Oxyrrhis Marina: Size Selectivity and Preference for Calcified Emiliania Huxleyi Cells AQUATIC MICROBIAL ECOLOGY Vol. 10: 307-313,1996 Published June 27 Aquat Microb Ecol l NOTE Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi 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 grazing on nanophythoplankton by the to algae 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, 0. marina also seems to be able to discriminate mixtures of differently sized algae: (1) Micromonas pusiUa (2 pm Equivalent Spherical Diameter), Emihania huxleyi between food species (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), Isochrysis galbana (5 pm ESD), ity in 0.marina grazing and (2) whether or not E. hux- Rhodomonas sp. (8 pm ESD). and Tetraselmis sp. (10 pm 0. leyi may form an exception within its size class. In con- ESD). 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. Oxyrrhis marina 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- KEY WORDS: Protozoa . Food selection - Prey size . Micro- nated 16 h light:8 h dark with 60 pE m-2 S-'. 0.marina phytoplankton . Coccoliths was fed Isochrysis galbana and Rhodomonas sp. In 3 incubation expenments Oxyrrhis marina (18 pm Equivalent Spherical Diameter, ESD) was offered dif- Heterotrophic dinoflagellates 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~unitythat 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 model organism 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 (pm3ml-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 Tetraselmis suecica 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 2 Fig. 1. Simultaneous mea- surement of different - a,.,.,. 1 algal specles by flow cyto- L / , , ] metry. (a) Expt 2. N: Nan- 0 1 ,, 100 =Q) nochloris sp.; I: Isochrysis galbana; R: Rhodomonas g': I0 sp.; T. Tetraselmis sp. m m b2 m (b) Expt 3. (c) Expt 3. Cal- cified and noncalcified l 10 100 100010000 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 lIsochrysis 0 6 12 18 24 30 36 42 48 0 6 12 18 24 30 36 42 48 time [h] time [h] 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.
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