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The Role of Mixotrophy in Pelagic Environments

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Molecular Ecology of Aquatic Microbes

Part of the book series: NATO ASI Series ((ASIG,volume 38))

Abstract

This paper reviews the occurrence and ecological importance of mixotrophic flagellates and ciliates in pelagic environments, particularly in marine ecosystems. Mixotrophy is here defined as the combination of photoautotrophic and heterotrophic nutrition in a single individual, often used in the restricted sense of combining photosynthesis and phagotrophy. Mixotrophic protists represent an alternative strategy that allows a shortcut between the traditional food web and the microbial loop. A large number of reports have been published on the ecological importance of mixotrophic flagellates in freshwater, yet only a few studies have been carried out in seawater. In contrast, most of the knowledge of mixotrophic ciliates comes from marine environments. Results from field studies have demonstrated that both mixotrophic flagellates and ciliates are commonly found in many marine environments, and mixotrophic flagellates can dominate the biomass of photoautotrophs and be responsible for the entire grazing of bacteria or protists. Results from laboratory experiments on factors controlling the degree of photoautotrophy/phagotrophy in flagellates are presented. Finally, we present a hypothesis for a growth strategy of bacterivorous mixotrophic flagellates.

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References

  • Andersson A, Falk S, Samuelsson G, Hagström, Å (1989) Nutritional Characteristics of a Mixotrophic Nanoflagellate, Ochromonas sp. Microb Ecol 17: 251–262

    Article  CAS  Google Scholar 

  • Auf dem Venne H (1990) Distribution of auto-, mixo-, and heterotrophic planktonic ciliates in the Greenland Sea in late spring and fall 1988. Comm Meet Int Cou Explor Sea C.M.-ICES/L:10

    Google Scholar 

  • Azam F, Fenchel T, Field J, Gray JS, Meyer-Reil LA and Thingstad F (1983) The ecological role of water column microbes in the sea. Mar Ecol Prog Ser 10: 257–263

    Article  Google Scholar 

  • Azam F and Fuhrmann JA (1984) Measurements of bacterioplankton growth in the sea and its regulation by environmental conditions:. In: Heterotrophic activity in the sea. Hobbie JE and Williams PJLeB (eds). Plenum Press New York 179–1196

    Google Scholar 

  • Bennett SJ, Sanders RW, Porter KG (1990) Heterotrophic, autotrophic and mixotrophic nanoflagellates: seasonal abundances and bacterivory in a eutrophic lake. Limnol Oceanogr 35: 1821–1832

    Article  Google Scholar 

  • Bernard C and Rassoulzadegan F (1994) Bacteria or microflagellates as a major food source for marine ciliates: possible implications for the microzooplankton. Mar Ecol Prog Ser 64: 147–155

    Article  Google Scholar 

  • Berninger U-G, Caron DA, Sanders RW (1992) Mixotrophic algae in three ice-covered lakes of the Pocono Mountains, U.S.A. Freshwater Biol 28: 263–272

    Article  Google Scholar 

  • Biecheler B (1936) Observation de la capture et la digestion des proies chez un péridinien vert. Comptes rendus des séances de la Société de Biologie 122: 1173–1175

    Google Scholar 

  • Biecheler B (1952) Recherches sur les Péridiniens. Bull Biol Fr Belg 36 (suppl.): 1–149

    Google Scholar 

  • Bird DF and Kalff J (1986) Bacterial Grazing by Planktonic Lake Algae. Science 231: 493–495

    Article  PubMed  CAS  Google Scholar 

  • Bird DJ and Kalff J (1987) Algal phagotrophy: Regulating factors and importance relative to photosynthesis in Dinobryon (Chrysophyceae). Limnol Oceanogr 32: 277–284

    Article  CAS  Google Scholar 

  • Bird DF and Kalff J (1989) Phagotrophic sustenance of a metalimnetic phytoplankton peak. Limnol Oceanogr 34: 155–162

    Article  Google Scholar 

  • Blackbourn DJ, Taylor FJR, Blackbourn J (1973) Foreign organelle retention by ciliates. J Protozool 20: 286–288

    Google Scholar 

  • Bockstahler KR and Coats DW (1993a) Spatial and Temporal Aspects of Mixotrophy in Chesapeake Bay Dinoflagellates. J Euk Microbiol 40(1): 49–60

    Article  Google Scholar 

  • Bockstahler KR and Coats DW (1993b) Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Mar Biol 116: 477–487

    Article  Google Scholar 

  • Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund, OH (1992) Incorporation of viruses into the budget of microbial C-transfer. A first approach. Mar Ecol Prog Ser 83: 273–280

    Article  Google Scholar 

  • Cachon M, Cachon J, Cosson J, Greuet C, Huitorel P (1991) Dinoflagellate flagella adopt various conformations in response to different needs. Biol Cell 71: 175–182

    Article  Google Scholar 

  • Caron AC, Porter KG, Sanders RW (1990) Carbon, nitrogen, and phosphorus budgets for the mixotrophic phytoflagellate Poterioochromonas malhamensis (Chrysophyceae) during bacterial ingestion. Limnol Oceanogr 35(2): 433–443

    Article  CAS  Google Scholar 

  • Caron AC, Sanders RW, Lim EL, Marrasé C, Amaral LA, Whitney S, Aoki RB, Porter KG (1993) Light-Dependent Phagotrophy in the Freshwater Mixotrophic Chrysophyte Dinobryon cylindricum. Microb Ecol 25: 93–111

    Google Scholar 

  • Currie DJ and Kalff J (1984) The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in seawater. Limnol Oceanogr 29: 311–321

    Article  CAS  Google Scholar 

  • Davies PG and Sieburth JMcN (1984) Estuarine and oceanic microflagellate predation of actively growing bacteria: Estimation by frequency of dividing-divided bacteria. Mar Ecol Prog Ser 19:237–246

    Article  Google Scholar 

  • Dale T (1987) Diel vertical distribution of planktonic ciliates in Lindaspollene, western Norway. Mar Microb Food Webs 2: 15–28

    Google Scholar 

  • Dodge JD and Crawford RM (1970) The morphology and fine structure of Ceratium hirundinella (Dinophyceae). J Phycol 6: 137–149

    Google Scholar 

  • Dolan JR (1992) Mixotrophy in ciliates: a review of Chlorella symbiosis and chloroplast retention. Mar Microb Food Webs 6: 115–132

    Google Scholar 

  • Droop MR (1963) Algae and invertebrates in symbiosis. Symp Soc Gen Microbiol 13: 171–199

    Google Scholar 

  • Estep KW, Davis PG, Keller MD, Sieburth JMcN (1986) How important are algal nanoflagellates in bacterivory? Limnol Oceanogr 31: 646–50

    Article  Google Scholar 

  • Fenchel T (1988) Marine plankton food chains. Ann Rev Ecol Syst 19: 19–38

    Article  Google Scholar 

  • Fenchel T (1991) Flagellate design and function. In: The Biology of Free-living Heterotrophic Flagellates. Patterson DJ and Larsen J:(eds) Syst Ass 45. Clarendon Press. Oxford 7–19

    Google Scholar 

  • Fenchel T and Bernard C (1993) Endosymbiotic purple nonsulphur bacteria in an anaerobic ciliated protozoan. FEMS Microbiol Lett 110: 21–25

    Article  CAS  Google Scholar 

  • Finlay BJ, Berninger U-G, Stewart LJ, Hindle RM, Davison W (1987) Some factors controlling the distribution of two pond-dwelling ciliates with algal symbionts (Frontonia vernalis and Euplotes daidaleos). J Protozool 34: 349–356

    Google Scholar 

  • Finlay BJ and Fenchel T (1989) Everlasting picnic for protozoa. New Scientist. 1671: 66–69

    Google Scholar 

  • Finlay BJ, Clarke KJ, Cowling AJ, Hindle RM, Rogerson A, Berninger U-G (1988) On the abundance and distribution of protozoa and their food in a productive freshwater pond. Europ J Protistol 23: 205–217

    Article  Google Scholar 

  • Gourret P (1883) Sur les Péridiniens du golfe de Marseille. Annales du musée d’histoire naturelle de Marseille. Zoologie. T. 1

    Google Scholar 

  • Green JC (1991) Phagotrophy in prymnesiophyte flagellates. In: The Biology of Free- living Heterotrophic Flagellates. Patterson, DJ and Larsen, (eds) J: Syst Ass 45. Clarendon Press. Oxford 21–38

    Google Scholar 

  • Haas LW (1982) Improved epifluorescence microscopy for observing planktonic microorganisms. Ann Inst Oceanogr, Paris 58: 261–266

    Google Scholar 

  • Hall JA, Barett DP, James MR (1993) The importance of phytoflagellate, heterotrophic flagellate and ciliate grazing on bacteria and picophytoplankton sized prey in a coastal marine environment. J Plankt Res 15(9): 1075–1086

    Article  Google Scholar 

  • Hällfors G and Niemi Ä (1974) A Chrysochromulina (Haptophyceae) bloom under the ice in the Tvärminne archipelago, southern coast of Finland. Memoranda Societatis pr Fauna et Flora fennica 50: 89–10

    Google Scholar 

  • Hansen PJ (1991) Dinophysis — a planktonic dinoflagellate genus which can act both as a prey and a predator of a ciliate. Mar Ecol Prog Ser 69: 201–204

    Article  Google Scholar 

  • Havskum H and Riemann B (unpubl.) The ecological importance of mixotrophic flagellates in the Bay of Aarhus, Denmark.

    Google Scholar 

  • Hobbie JE and Williams PJLeB (1984): Heterotrophic activity in the sea. Plenum Press. New York

    Google Scholar 

  • Hofeneder H (1930) Über de animalische Ernährung von Ceratium hirundinella O.F. Müller und über die Rolle des Kernes bei dieser Zellfunktion. Arch Protistenkunde 71: 1–32

    Google Scholar 

  • Ishida Y and Kimura B (1986) Photosynthetic phagotrophy of Chrysophyceae: evolutionary aspects. Microbiological Sciences 3(5): 132–135

    PubMed  CAS  Google Scholar 

  • Jacobson D and Anderson D (1986) Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J Phycol 22: 249–258

    Article  Google Scholar 

  • Jones HLJ, Leadbeater BSC, Green, JC (1993) Mixotrophy in marine species of Chrysochromulina (Prymnesiophyceae): Ingestion and digestion of a small green flagellate. J Mar Biol Ass UK 73: 283–296

    Article  Google Scholar 

  • Jonsson PR (1987) Photosynthetic assimilation of inorganic carbon in marine oligotrich ciliates (Ciliophora, Oligotrichina). Mar Microb Food Webs 2: 55–68

    CAS  Google Scholar 

  • Jumars P, Penry DL, Baross JA, Perry MJ, Frost BW (1989) Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep-Sea Res. 36: 483–495

    Article  CAS  Google Scholar 

  • Kawachi M, Inouye I, Maeda O, Chihara M (1991) The haptonema as a food-capturing device: observations on Chrysochromulina hirta (Prymnesiophyceae). Phycologia 30(6): 563–573

    Article  Google Scholar 

  • Kawakami H (1991) An endosymbiotic Chlorella-bearing ciliate: Platyophora chlorelligera Kawakami 1989. Eur J Protistol 26: 245–255

    Article  Google Scholar 

  • Kugrens P and Lee RE (1990) Ultrastructural Evidence for Bacterial Incorporation and Myxotrophy in the Photosynthetic Cryptomonad Chroomonas pochmanni Huber-Pestalozzi (Cryptomonadida). J Protozool 37(4): 263–267

    Google Scholar 

  • Larsen J (1988) An ultrastructural study of Amphidiniumpoecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27: 366–377.

    Article  Google Scholar 

  • Laval-Peuto M (1975) Cortex, perilemme et reticulum vésiculeux de Cyttarocylis brandti (Cilié Tintinnide). Les cilies ê périlemme. Protistologica 11: 83–98

    Google Scholar 

  • Laval-Peuto M (1991) Symbiose plastidiale et Mixotrophie des Ciliés planctoniques marins oligotrichina (Ciliophora). Thèse Doctorat Etat, Université Nice-Sophia Antipolis. Fasc. 1: mémoire, 176 p. Fasc. 2: 13 articles, 191 p.

    Google Scholar 

  • Laval-Peuto, M (1992) Plastidic protozoa. In:Algae and symbioses. Reisser, W (ed.) Biopress Ltd, Bristol, 471–499

    Google Scholar 

  • Laval-Peuto M and Febvre M (1986) On plastid symbiosis in Tontonia appendiculariformis (Ciliophora, Oligotrichina). Bio Systems 19: 137–158

    Article  PubMed  CAS  Google Scholar 

  • Laval-Peuto M and Rassoulzadegan F (1988) Autofluorescence of marine planktonic Oligotrichina and other ciliates. Hydrobiologia 159: 99–110

    Article  Google Scholar 

  • Laval-Peuto M and Salvano P (1991) Cytochemistry of polysaccharides stored by ciliates in symbiosis with plastids (Ciliophora, Oligotrichina). Symbiosis (submitted)

    Google Scholar 

  • Laval-Peuto M, Salvano P, Gayol P, Greuet C (1986) Mixotrophy in marine planktonic ciliates: ultrastructural study of Tontonia appendiculariformis (Ciliophora, Oligotrichina). Mar Microb Food Webs 1: 81–104

    Google Scholar 

  • Lindeman RL (1942) The trophic dynamic aspect of ecology. Ecology 23: 399–418

    Article  Google Scholar 

  • Lindholm T (1985) Mesodinium rubrum — a unique photosynthetic ciliate. Adv Aqua Microb 3: 1–48

    Google Scholar 

  • Lindholm T, Lindroos P, Murk A-C (1988) Ultrastructure of the photosynthetic ciliate Mesodinium rubrum. BioSystems 21: 141–149

    Article  PubMed  CAS  Google Scholar 

  • Lindholm T and Murk, A-C (1989) Symbiotic algae and plastids in planktonic ciliates Memoranda Soc Fauna Flora Fennica 65: 17–22

    Google Scholar 

  • Lopez E (1979) Algal chloroplasts in the protoplasm of three species of benthic foraminifera: taxonomic affinity, viability and persistence. Mar Biol 53: 201–211

    Article  CAS  Google Scholar 

  • McManus GB and Fuhrmann JA (1986a) Bacterivory in seawater studied with the use of inert fluorescent particles. Limnol Oceanogr 31: 420–426

    Article  Google Scholar 

  • McManus GB and Fuhrmann JA (1986b) Photosynthetic pigments in the ciliate Laboea strobila from Long Island Sound, USA. J Plankt Res 8: 317–327

    Article  Google Scholar 

  • Moestrup, Ø and Andersen, RA (1991) Organization of heterotrophic heterokonts. In The Biology of Free-living Heterotrophic Flagellates. Patterson DJ and Larser J (eds): Syst Ass 45. Clarendon Press. Oxford: 333–360

    Google Scholar 

  • Nielsen TG and Kiørboe T (1994) Regulation of Zooplankton biomass and production in a temperate, coastal ecosystem. 2. Ciliates. Limnol Oceanogr 39: 508–519

    Article  Google Scholar 

  • Nyggard K and Tobiesen A (1993) Bacterivory in algae: A survival strategy during nutrient limitation. Limnol Oceanogr 38(2): 273–279

    Article  Google Scholar 

  • Olrik K and Nauwerck A (1993) Stress and disturbance in the phytoplanktor community of a shallow, hypertrophic lake. Hydrobiologia 249: 15–24

    Article  CAS  Google Scholar 

  • Parke M, Manton I, Clarke B (1956) Studies on marine flagellates. III. Three furthei species of Chrysochromulina. J Mar Biol Ass UK 35: 387–414

    Article  Google Scholar 

  • Pascher A (1917) Flagellaten und Rhizopoden in ihren gegenseitigen Beziehungen Archiv für Protistenkunde 38: 1–87

    Google Scholar 

  • Patterson DJ and Dürrschmidt M (1987) Selective retention of chloroplasts by algivorous heliozoa: Fortuitous chloroplast symbiosis? Eur op J Protistol 23: 51–55

    Article  Google Scholar 

  • Pengerud B, Skjoldal EF, Thingstad TF (1987) The reciprocal interaction betweer degradation of glucose and ecosystem structure. Studies in mixed chemostat cultures of marine bacteria, algae, and bacterivorous nanoflagellates. Mar Ecol Prog Ser 35:111–117

    Article  CAS  Google Scholar 

  • Porter KG (1988) Phagotrophic phytoflagellates in microbial food webs Hydrobiologia 159: 89–97

    Article  Google Scholar 

  • Pringsheim EG (1952) On the nutrition of Ochromonas. Quart J Microscopical Soc 93 (1): 71–96

    Google Scholar 

  • Provasoli L (1977) Cultivation of animals. In: Marine Ecology, Vol. 3 Kinne, O (ed) Wiley, New York 1295–1320.

    Google Scholar 

  • Putt M (1990a) Metabolism of photosynthate in the chloroplast-retaining ciliate Laboea strobila. Mar Ecol Prog Ser 60: 271–282

    Article  CAS  Google Scholar 

  • Putt M (1990b) Abundance, chlorophyll content and photosynthetic rates of ciliates ir the Nordic Seas during summer. Deep Sea Res 37: 1713–1731

    Article  Google Scholar 

  • Rassoulzadegan F, Laval-Peuto M, Sheldon RW (1988) Partitioning of the food ratior of marine ciliates between pico- and nanoplankton. Hydrobiologia 159: 75–88

    Article  Google Scholar 

  • Reisser W (1986) Endosymbiontic associations of freshwater protozoa and algae. In Progress in Protistology. Corliss JO and Patterson DJ (eds) Biopress Ltd Bristol 195–214

    Google Scholar 

  • Riemann, B and Sondergaard, M (1986) Regulation of bacterial secondary productior in two eutrophic lakes and in experimental enclosures. J Plankt Res 8: 519–536

    Article  CAS  Google Scholar 

  • Rogerson A, Finlay BJ, Berninger U-G (1989) Sequestered chloroplasts in the freshwater ciliate Strombidium viride (Ciliophora: Oligotrichida). Trans Amer Micr Soc 108: 117–126

    Article  Google Scholar 

  • Rublee PA and Gallegos CL (1989) Use of fluorescently labelled algae (FLA) to estimate microzooplankton grazing. Mar Ecol Prog Ser 51: 221–227

    Article  Google Scholar 

  • Salonen K and Jokinen S (1988) Flagellate grazing on bacteria in a small dystrophic lake. Hydrobiologia 161: 203–209

    Article  Google Scholar 

  • Sanders RW (1991a) Trophic strategies among heterotrophic flagellates. In:The Biology of Free-living Heterotrophic Flagellates Patterson DJ and Larsen J (eds). Syst Ass. 45 Clarendon Press Oxford: 21–38

    Google Scholar 

  • Sanders RW (1991b) Mixotrophic protists in marine and freshwater ecosystems. J Protozool 38: 76–81

    Google Scholar 

  • Sanders RW, Porter KG, Bennett SJ, De Biase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34: 673–687

    Article  Google Scholar 

  • Sanders RW, Porter KG, Caron DA (1990) Relationship Between Phototrophy and Phagotrophy in the Mixotrophic Chrysophyte Poterioochromonas malhamensis. Micro Ecol 19: 97–109

    Article  Google Scholar 

  • Schnepf E, Deichgräber G, Drebes G (1985) Food uptake and the fine structure of the dinophyte Paulsenella sp., an ectoparasite of marine diatoms. Protoplasma 124: 188–204

    Article  Google Scholar 

  • Schnepf E, Winter S, Mollenhauer D (1989) Gymnodinium aeruginosum (Dinophyta): a blue-green dinoflagellate with a vestigial, anucleate, cryptophycean endosymbiont. Pl Syst Evol 164: 75–91

    Article  Google Scholar 

  • Smetacek VS (1981) The annual cycle of protozooplankton in the Kiel Bight. Mar Biol 63: 1–11

    Article  Google Scholar 

  • Spero HJ (1982) Phagotrophy in Gymnodinium fungiforme (Pyrrhophyta): the pedunkel as an organelle of ingestion. J Phycol 18: 356–360

    Article  Google Scholar 

  • Stoecker DK (1991) Mixotrophy in marine planktonic ciliates: physiological and ecological aspects of plastid retention by oligotrichs. In: Protozoa and their role in marine processes Reid PC, Turley CM, Burkill PH (eds), G25. NATO ASI Series, Springer-Verlag, Berlin, Heidelberg 161–179

    Chapter  Google Scholar 

  • Stoecker DK, Buck KR, Putt M (1992) Changes in the sea-ice brine community during the spring-summer transition, McMurdo Sound, Antarctica. I. Photosynthetic protists. Mar Ecol Prog Ser 84: 265–278

    Article  Google Scholar 

  • Stoecker, DK and Michaels, AE (1991) Respiration, photosynthesis and carbon metabolism in planktonic ciliates. Mar Biol 108: 441–447

    Article  CAS  Google Scholar 

  • Stoecker DK, Michaels AE, Davis LH (1987) Large proportion of marine planktonic ciliates found to contain functional chloroplasts. Nature 326: 790–792

    Article  Google Scholar 

  • Stoecker DK and Silver MW (1987) Chloroplast retention by marine planktonic ciliates. In: Endocytobiology III, Vol 503 Lee, JJ and Fredericks, J (eds), Ann New York Acad Sci 562–565

    Google Scholar 

  • Stoecker DK, Silver MW, Michaels AE, Davis LH (1988/1989) Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, Oligotrichida). Mar Microb Food Webs 3: 79–100

    Google Scholar 

  • Stoecker DK, Taniguchi A, Michaels AE (1989) Abundance of autotrophic, mixotrophic and heterotrophic planktonic ciliates in shelf and slope waters. Mar Ecol Prog Ser 50: 241–254

    Article  Google Scholar 

  • Suttle CA, Fuhrman JA, Capone DG (1990) Rapid ammonium cycling and concentration-dependent partitioning of ammonium and phosphate: Implications for carbon transfer in planktonic communities. Limnol Oceanogr 35:424–433

    Article  CAS  Google Scholar 

  • Swale EMF (1969) A study of the nanoplankton flagellate Pedinella hexacostata Vysotskii by light and electron microscopy. Br Phycol J 4: 65–86

    Article  Google Scholar 

  • Taylor FJR (1982) Symbioses in marine microplankton. Ann. Inst Oceanogr., Paris 58: 6190

    Google Scholar 

  • Thingstad TF and Pengerud B (1985) Fate and effect of allochthonous organic material in aquatic microbial ecosystems. An analysis based on chemostat theory. Mar Ecol Prog Ser 21:47–62

    Article  Google Scholar 

  • Thingstad TF, Skjoldal EF, Bohne, RA (1993) Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway. Mar Ecol Prog Ser 99:239–259

    Article  CAS  Google Scholar 

  • Tranvik LJ, Porter KG, Sieburth, JMcN (1989) Occurrence of bacterivory in Cryptomonas, a common freshwater phytoplankter. Oecologia 78: 473–476

    Article  Google Scholar 

  • Verity PG and Vernet M (1992): Microzooplankton grazing, pigments and composition of plankton communities during late spring in two Norwegians fjords. Sarsia 77: 263–274

    Google Scholar 

  • Wawrik F (1970) Mixotrophie bei Cryptomonas borealis Skuja. Arch Protistenk 112: 312–313

    Google Scholar 

  • Weis DS (1982) Protozoal Symbionts. In: Experimental Microbial Ecology Burns RG and Slater JH, (eds). pp. 320–341, Blackwell

    Google Scholar 

  • Wehr JD, Brown LM, O’Grady K (1985) Physiological ecology of the bloom-forming alga Chrysochromulina breviturrita (Prymnesiophyceae) from lakes influenced by acid precipitation. Can J Bot 63: 2231–2239

    Article  CAS  Google Scholar 

  • Wetherbee R and Andersen RA (1992) Flagella of a chrysophycean alga play an active role in prey capture and selection. Direct observations on Epipyxis pulchra using image enhanced video microscopy. Protoplasma 166: 1–7

    Article  Google Scholar 

  • Wilcox LW and Wedemeyer GJ (1991) Phagotrophy in the Freshwater, Photosynthetic Dinoflagellate Amphidinium cryophilum. J Phycol 27: 600–609

    Article  Google Scholar 

  • Wilson EO and Bossert WH (1971) A primer of population biology. Sinauer Associates Inc. Publishers. Stamford Connecticut

    Google Scholar 

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Authors and Affiliations

  1. The International Agency for 14Carbon Determination, VKI, Agern Allé 11, DK-2970, Hørsholm, Denmark

    Bo Riemann & Harry Havskum

  2. Dept. of Microbiology, University of Bergen, Jahnebakken 5, N-5020, Bergen, Norway

    Frede Thingstad

  3. Marine Biological Laboratory, University of Copenhagen, Strandpromenaden 5, DK-3000, Helsingør, Denmark

    Catherine Bernard

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  1. Bo Riemann
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  2. Harry Havskum
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  3. Frede Thingstad
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  4. Catherine Bernard
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Editors and Affiliations

  1. Plymouth Marine Laboratory, Natural Environment Research Council, Prospect Place, The Hoe, PL1 3DH, Plymouth, UK

    Ian Joint

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Riemann, B., Havskum, H., Thingstad, F., Bernard, C. (1995). The Role of Mixotrophy in Pelagic Environments. In: Joint, I. (eds) Molecular Ecology of Aquatic Microbes. NATO ASI Series, vol 38. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79923-5_6

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  • DOI: https://doi.org/10.1007/978-3-642-79923-5_6

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