1932

Abstract

Mixotrophs are important components of the bacterioplankton, phytoplankton, microzooplankton, and (sometimes) zooplankton in coastal and oceanic waters. Bacterivory among the phytoplankton may be important for alleviating inorganic nutrient stress and may increase primary production in oligotrophic waters. Mixotrophic phytoflagellates and dinoflagellates are often dominant components of the plankton during seasonal stratification. Many of the microzooplankton grazers, including ciliates and Rhizaria, are mixotrophic owing to their retention of functional algal organelles or maintenance of algal endosymbionts. Phototrophy among the microzooplankton may increase gross growth efficiency and carbon transfer through the microzooplankton to higher trophic levels. Characteristic assemblages of mixotrophs are associated with warm, temperate, and cold seas and with stratification, fronts, and upwelling zones. Modeling has indicated that mixotrophy has a profound impact on marine planktonic ecosystems and may enhance primary production, biomass transfer to higher trophic levels, and the functioning of the biological carbon pump.

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2017-01-03
2024-03-28
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Literature Cited

  1. Andersen KH, Aksnes DL, Berge T, Fiksen Ø, Visser A. 2015. Modelling emergent trophic strategies in plankton. J. Plankton Res. 37:862–68 [Google Scholar]
  2. Anderson OR. 1993. The trophic role of planktonic foraminifera and radiolaria. Mar. Microb. Food Webs 7:31–51 [Google Scholar]
  3. Arenovski AL, Lim EL, Caron DA. 1995. Mixotrophic nanoplankton in oligotrophic surface waters of the Sargasso Sea may employ phagotrophy to obtain major nutrients. J. Plankton Res. 17:801–20 [Google Scholar]
  4. Assmy P, Cisewski B, Henjes J, Klaas C, Montresor M, Smetacek V. 2014. Response of the protozooplankton assemblage during the European Iron Fertilization Experiment (EIFEX) in the Antarctic circumpolar current. J. Plankton Res. 36:1175–89 [Google Scholar]
  5. Baretta-Bekker JG, Baretta JW, Hansen AS, Riemann B. 1998. An improved model of carbon and nutrient dynamics in the microbial food web in marine enclosures. Aquat. Microb. Ecol. 14:91–108 [Google Scholar]
  6. AWH, Anderson OR, Faber WW Jr., Caron DA. 1983. Sequence of morphological and cytoplasmic changes during gametogenesis in the planktonic foraminifer Globigerinoides sacculifer (Brady). Micropaleontology 29:310–25 [Google Scholar]
  7. Béja O, Suzuki T. 2008. Photoheterotrophic marine procaryotes. Microbial Ecology of the Oceans DL Kirchman 131–57 Hoboken, NJ: John Wiley & Sons, 2nd ed.. [Google Scholar]
  8. Bell EM, Laybourn-Parry J. 2003. Mixotrophy in the Antarctic phytoflagellate, Pyramimonas gelidicola (Chlorophyta: Prymnesiophyceae). J. Phycol. 39:644–49 [Google Scholar]
  9. Biard T, Stemmann L, Picheral M, Mayot N, Vandromme P. et al. 2016. In situ imaging reveals the biomass of large protists in the global ocean. Nature 532:504–7 [Google Scholar]
  10. Bird DF, Kalff J. 1986. Bacterial grazing by planktonic lake algae. Science 231:493–95 [Google Scholar]
  11. Blackford JC, Allen JI, Gilbert FJ. 2004. Ecosystem dynamics at six contrasting sites: a generic modelling study. J. Mar. Syst. 52:191–215 [Google Scholar]
  12. Blossom H, Daugbjerg N, Hansen PJ. 2012. Toxic mucus traps: a novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful Algae 17:40–53 [Google Scholar]
  13. Burkholder JM, Glibert PM, Skelton HM. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93 [Google Scholar]
  14. Calbet A, Bertos M, Fuentes-Grünewald C, Alacid E, Figueroa R. et al. 2011. Interspecific variability in Karlodinium veneficum: growth rates, mixotrophy, and lipid composition. Harmful Algae 10:654–67 [Google Scholar]
  15. Calbet A, Saiz E. 2005. The ciliate-copepod link in marine ecosystems. Aquat. Microb. Ecol. 38:157–67 [Google Scholar]
  16. Caron DA, Michaels AF, Swanberg NR, Howse FA. 1995. Primary productivity by symbiont- bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J. Plankton Res. 17:103–29 [Google Scholar]
  17. Caron DA, Porter KG, Sanders RW. 1990. Carbon, nitrogen and phosphorus budgets for the mixotrophic phytoflagellate Poterioochromonas malhamensis (Chrysophyseae) during bacterial ingestion. Limnol. Oceanogr. 35:433–43 [Google Scholar]
  18. Caron DA, Swanberg NR. 1990. The ecology of planktonic sarcodines. Rev. Aquat. Sci. 3:147–80 [Google Scholar]
  19. Christaski U, Obernosterer I, Van Wambeke F, Veldhuis M, Garcia N, Catala P. 2008. Microbial food web structure in a naturally iron-fertilized area in the Southern Ocean (Kerguelen Plateau). Deep-Sea Res. II 55:706–19 [Google Scholar]
  20. Crawford DW. 1989. Mesodinium rubrum: the phytoplankter that wasn't. Mar. Ecol. Prog. Ser. 58:161–74 [Google Scholar]
  21. Crawford DW, Purdie DA, Lockwood APM, Weissman P. 1997. Recurrent red-tides in the Southampton water estuary caused by the photosynthetic ciliate Mesodinium rubrum. Estuar. Coast. Shelf Sci. 45:799–812 [Google Scholar]
  22. Crawford DW, Stoecker DK. 1996. Carbon content, dark respiration and mortality of the mixotrophic planktonic ciliate Strombidium capitatum. Mar. Biol. 126:415–22 [Google Scholar]
  23. Czypionka T, Vargas CA, Silva N, Daneri G, González HE, Iriate JL. 2011. Importance of mixotrophic nanoplankton in Aysén Fjord (Southern Chile) during austral winter. Cont. Shelf Res. 31:216–24 [Google Scholar]
  24. Davidson AT, Scott FJ, Nash GV, Wright SW, Raymond B. 2010. Physical and biological control of protistan community composition, distribution and abundance in the seasonal ice zone of the Southern Ocean between 30 and 80°E. Deep-Sea Res. II 57:828–48 [Google Scholar]
  25. de Vargas C, Audic S, Henry N, Decelle J, Mahé F. et al. 2015. Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605 [Google Scholar]
  26. Decelle J, Probert I, Bittner L, Desdevises Y, Colin S. et al. 2012. An original mode of symbiosis in open ocean plankton. PNAS 109:18000–5 [Google Scholar]
  27. Dolan JR, Marrase C. 1995. Planktonic ciliate distribution relative to a deep chlorophyll maximum: Catalan Sea, N.W. Mediterranean, June 1993. Deep-Sea Res. I 42:1965–87 [Google Scholar]
  28. Dolan JR, Pérez MT. 2000. Costs, benefits and characteristics of mixotrophy in marine oligotrichs. Freshw. Biol. 45:227–38 [Google Scholar]
  29. Dutz J, Peters J. 2008. Importance and nutritional value of large ciliates for the reproduction of Acartia clausi during the post spring-bloom period in the North Sea. Aquat. Microb. Ecol. 50:261–77 [Google Scholar]
  30. Eiler A. 2006. Evidence for the ubiquity of mixotrophic bacteria in the upper ocean: implications and consequences. Appl. Environ. Microbiol. 72:7431–37 [Google Scholar]
  31. Esteban GF, Fenchel T, Finlay BJ. 2010. Mixotrophy in ciliates. Protist 161:621–41 [Google Scholar]
  32. Farnelid H, Tarangkoon W, Hansen G, Hansen PJ, Riemann L. 2010. Putative N2-fixing heterotrophic bacteria associated with dinoflagellate–Cyanobacteria consortia in the low-nitrogen Indian Ocean. Aquat. Microb. Ecol. 61:105–17 [Google Scholar]
  33. Figueiredo GM, Nash RDM, Montagnes DJS. 2007. Do protozoa contribute significantly to the diet of larval fish in the Irish Sea?. J. Mar. Biol. Assoc. UK 87:843–50 [Google Scholar]
  34. Fileman E, Smith T, Harris R. 2007. Grazing by Calanus helgolandricus and Para-Pseudocalanus spp. on phytoplankton and protozooplankton during the spring bloom in the Celtic Sea. J. Exp. Mar. Biol. Ecol. 348:70–84 [Google Scholar]
  35. Flynn KJ. 2010. Ecological modelling in a sea of variable stoichiometry: dysfunctionality and the legacy of Redfield and Monod. Prog. Oceanogr. 84:52–65 [Google Scholar]
  36. Flynn KJ, Hansen PJ. 2013. Cutting the canopy to defeat the “selfish gene”; conflicting selection pressures for the integration of phototrophy in mixotrophic protists. Protist 164:811–23 [Google Scholar]
  37. Flynn KJ, Mitra A. 2009. Building the “perfect beast”: modelling mixotrophic plankton. J. Plankton Res. 31:965–92 [Google Scholar]
  38. Flynn KJ, Stoecker DK, Mitra A, Raven JA, Glibert PM. et al. 2013. Misuse of the phytoplankton zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J. Plankton Res. 35:3–11 [Google Scholar]
  39. Foster RA, Carpenter EJ, Bergman B. 2006. Unicellular cyanobionts in open ocean dinoflagellates, radiolarians, and tintinnids: ultrastructural characterization and immune-localization of phycoerythrin and nitrogenase. J. Phycol. 42:453–63 [Google Scholar]
  40. Franks PJS. 2009. Planktonic ecosystem models: perplexing parameterizations and a failure to fail. J. Plankton Res. 31:1299–306 [Google Scholar]
  41. Franzè G, Lavrentyev PJ. 2014. Microzooplankton growth rates examined across a temperature gradient in the Barents Sea. PLOS ONE 9:e86429 [Google Scholar]
  42. Fulton EA, Parslow JS, Smith ADM, Johnson CR. 2004. Biogeochemical marine ecosystem models II. The effect of physiological detail on model performance. Ecol. Model. 173:371–406 [Google Scholar]
  43. Furuya K, Saito H, Sriwoon R, Omura T, Furio EE. et al. 2006. Vegetative growth of Noctiluca scintillans containing the endosymbiont Pedinomonas noctilucae. Afr. J. Mar. Sci. 28:305–8 [Google Scholar]
  44. Gaither MR, Rowan R. 2010. Zooxanthellar symbiosis in planula larvae of the coral Pocillopora damicornis. J. Exp. Mar. Biol. Ecol. 386:45–53 [Google Scholar]
  45. Garcia-Cuetos L, Moestrup Ø, Hansen PJ. 2012. Studies on the genus Mesodinium II. Ultrastructural and molecular investigations of five marine species help clarifying the taxonomy. J. Eukaryot. Microbiol. 59:374–400 [Google Scholar]
  46. Gast RJ, Caron DA. 2001. Photosymbiotic associations in planktonic foraminifera and radiolaria. Hydrobiologia 461:1–7 [Google Scholar]
  47. Gast RJ, Moran DM, Beaudoin DJ, Blythe JN, Dennett MR, Caron DA. 2006. Abundance of a novel dinoflagellate phylotype in the Ross Sea, Antarctica. J. Phycol. 42:233–42 [Google Scholar]
  48. Gast RJ, Moran DM, Dennett MR, Caron DA. 2007. Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition?. Environ. Microbiol. 9:39–45 [Google Scholar]
  49. Gerea M, Saad JF, Izaguirre I, Queimaliños C, Gasol JM, Unrein F. 2016. Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments. Aquat. Microb. Ecol. 76:219–32 [Google Scholar]
  50. Giovannoni SJ, Bibbs L, Cho JC, Stapels MD, Desiderio R. et al. 2005. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438:82–85 [Google Scholar]
  51. Gomes HDR, Goes JI, Matondkar SGP, Buskey EJ, Basu S. et al. 2014. Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia. Nat. Commun. 5:4862 [Google Scholar]
  52. Gómez-Consarnau L, Akram N, Lindell K, Pedersen A, Neutze R. et al. 2010. Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLOS Biol. 8:e1000358 [Google Scholar]
  53. Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A. et al. 2016. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532:465–70 [Google Scholar]
  54. Guo Z, Zhang H, Lin S. 2014. Light-promoted rhodopsin expression and starvation survival in the marine dinoflagellate Oxyrrhis marina. PLOS ONE 9:e114941 [Google Scholar]
  55. Gustafson DE, Stoecker DK, Johnson MD, Van Heukelem WF, Sneider K. 2000. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature 405:1049–52 [Google Scholar]
  56. Haeckel E. 1887. Report on the Radiolaria collected by H.M.S. Challenger during the years 1873–1876. The Voyage of H.M.S. Challenger CW Thompson, J Murray 1–1760 London: Her Majesty's Station. Off. [Google Scholar]
  57. Hall JA, Barrett 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. Plankton Res. 15:1075–86 [Google Scholar]
  58. Hansen PJ. 2011. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58:203–14 [Google Scholar]
  59. Hansen PJ, Fenchel T. 2006. The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont. Mar. Biol. Res. 2:169–77 [Google Scholar]
  60. Hansen PJ, Miranda L, Azanza R. 2004. Green Noctiluca scintillans: a dinoflagellate with its own greenhouse. Mar. Ecol. Prog. Ser. 275:79–87 [Google Scholar]
  61. Hansen PJ, Moldrup M, Tarangkoon W, Garcia-Cuentos L, Moestrup Ø. 2012. Direct evidence for symbiont sequestration in the marine red tide ciliate Mesodinium rubrum. Aquat. Microb. Ecol. 66:63–75 [Google Scholar]
  62. Harrison PJ, Furuya K, Glibert PM, Xu J, Liu HB. et al. 2011. Geographical distribution of red and green Noctiluca scintillans. Chin. J. Oceanol. Limnol. 29:807–31 [Google Scholar]
  63. Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH. et al. 2012. Mixotrophic basis of Atlantic oligotrophic ecosystems. PNAS 109:5756–60 [Google Scholar]
  64. Hartmann M, Zubkov MV, Scanlan DJ, Lepère C. 2013. In situ interactions between photosynthetic picoeukaryotes and bacterioplankton in the Atlantic Ocean: evidence for mixotrophy. Environ. Microbiol. Rep. 5:835–40 [Google Scholar]
  65. Hauruseu D, Koblizek M. 2012. Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl. Environ. Microbiol. 78:7414–19 [Google Scholar]
  66. Havskum H, Riemann B. 1996. Ecological importance of bacterivorous, pigmented flagellates (mixotrophs) in the bay of Aarhus, Denmark. Mar. Ecol. Prog. Ser. 137:251–63 [Google Scholar]
  67. Herfort L, Peterson TD, McCue LA, Crump BC, Prahl FG. et al. 2011. Myrionecta rubra population genetic diversity and its cryptophyte chloroplast specificity in recurrent red tides in the Columbia River estuary. Aquat. Microb. 62:85–97 [Google Scholar]
  68. Herfort L, Peterson TD, Prahl FG, McCue LA, Needoba JA. et al. 2012. Red waters of Myrionecta rubra are biogeochemical hotspots for the Columbia River estuary with impacts on primary/secondary productions and nutrient cycles. Estuar. Coasts 35:878–91 [Google Scholar]
  69. Jakobsen HH, Hansen PJ, Larsen J. 2000. Growth and grazing responses of two chloroplast-retaining dinoflagellates: effects of irradiance and prey species. Mar. Ecol. Prog. Ser. 201:121–28 [Google Scholar]
  70. Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH. 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci 45:65–91 [Google Scholar]
  71. Johnson MD. 2015. Inducible mixotrophy in the dinoflagellate Prorocentrum minimum. J. Eukaryot. Microbiol. 62:431–43 [Google Scholar]
  72. Johnson MD, Oldach D, Delwiche CF, Stoecker DK. 2007. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426–28 [Google Scholar]
  73. Johnson MD, Stoecker DK. 2005. Role of feeding in growth and photophysiology of Myrionecta rubra. Aquat. Microb. Ecol. 39:303–12 [Google Scholar]
  74. Johnson MD, Tengs T, Oldach D, Stoecker DK. 2006. Sequestration, performance, and functional control of cryptophyte plastids in the ciliate Myrionecta rubra (Ciliophora). J. Phycol. 42:1235–46 [Google Scholar]
  75. Jones HLJ. 1997. A classification of mixotrophic protists based on their behavior. Freshw. Biol. 37:35–43 [Google Scholar]
  76. Jonsson PR. 1987. Photosynthetic assimilation of inorganic carbon in marine oligotrich ciliates (Ciliophora, Oligotrichina). Mar. Microb. Food Webs 2:55–68 [Google Scholar]
  77. Kim M, Nam SW, Shin W, Coats DW, Park MG. 2012. Dinophysis caudata (Dinophyceae) sequesters and retains plastids from the mixotrophic ciliate prey Mesodinium rubrum. J. Phycol. 48:569–79 [Google Scholar]
  78. Kirchman DL, Hanson TE. 2013. Bioenergetics of photoheterorophic bacteria in the oceans. Environ. Microbiol. Rep. 5:188–99 [Google Scholar]
  79. Kooijman SALM, Dijkstra HA, Kooi BW. 2002. Light-induced mass turnover in a mono-species community of mixotrophs. J. Theor. Biol. 214:233–54 [Google Scholar]
  80. Kremer P, Costello J, Kremer J, Canino M. 1990. Significance of photosynthetic endosymbionts to the carbon budget of the scyphomedusa Linuche unguiculata. Limnol. Oceanogr. 35:609–24 [Google Scholar]
  81. Landry MR, Calbet A. 2004. Microzooplankton production in the oceans. ICES J. Mar. Sci. 61:501–7 [Google Scholar]
  82. Lasek-Nesselquist E, Wisecaver JH, Hackett JD, Johnson MD. 2015. Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum. BMC Genom. 16:805 [Google Scholar]
  83. Levinsen H, Nielsen TG, Hansen BW. 2000a. Annual succession of marine pelagic protozoans in Disko Bay, West Greenland, with emphasis on winter dynamics. Mar. Ecol. Prog. Ser. 206:119–34 [Google Scholar]
  84. Levinsen H, Turner JT, Nielsen TG, Hansen BW. 2000b. On the trophic coupling between protists and copepods in arctic marine ecosystems. Mar. Ecol. Prog. Ser. 204:65–77 [Google Scholar]
  85. Li A, Stoecker DK, Adolf JE. 1999. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 19:163–76 [Google Scholar]
  86. Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S. et al. 2015. Determinants of community structure in the global plankton interactome. Science 348:1262073 [Google Scholar]
  87. Lindholm T. 1985. Mesodinium rubrum—a unique photosynthetic ciliate. Adv. Aquat. Microbiol. 3:1–48 [Google Scholar]
  88. Maranger R, Bird DF, Price NM. 1998. Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396:248–51 [Google Scholar]
  89. McManus GB, Schoener DM, Haberlandt K. 2012. Chloroplast symbiosis in a marine ciliate: ecophysiology and the risks and rewards of hosting foreign organelles. Front. Microbiol. 3:321 [Google Scholar]
  90. Mitra A, Castellani C, Gentleman WC, Jónasdóttir SH, Flynn KJ. et al. 2014a. Bridging the gap between marine biogeochemical and fisheries sciences; configuring the zooplankton link. Prog. Oceanogr. 129:176–99 [Google Scholar]
  91. Mitra A, Flynn KJ. 2010. Modelling mixotrophy in harmful algal blooms: more or less the sum of the parts?. J. Mar. Syst. 83:158–69 [Google Scholar]
  92. Mitra A, Flynn KJ, Burkholder JM, Berge T, Calbet A. et al. 2014b. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11:995–1005 [Google Scholar]
  93. Mitra A, Flynn KJ, Tillmann U, Raven J, Caron D. et al. 2016. Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition; incorporation of diverse mixotrophic strategies. Protist 167:106–20 [Google Scholar]
  94. Moeller HV, Johnson MD, Falkowski PG. 2011. Photoacclimation in the phototrophic marine ciliate Mesodinium rubrum (Ciliophora). J. Phycol. 47:324–32 [Google Scholar]
  95. Moorthi S, Caron DA, Gast RJ, Sanders RW. 2009. Mixotrophy: a widespread and important ecological strategy for planktonic and sea-ice nanoflagellates in the Ross sea, Antarctica. Aquat. Microb. Ecol. 54:269–77 [Google Scholar]
  96. Muscatine L, Wilkerson FP, McCloskey LR. 1986. Regulation of population density of symbiotic algae in a tropical marine jellyfish (Mastigias sp.). Mar. Ecol. Prog. Ser. 32:279–90 [Google Scholar]
  97. Nielsen LT, Krock B, Hansen PJ. 2012. Effects of light and food availability on toxin production, growth and photosynthesis in Dinophysis acuminata. Mar. Ecol. Prog. Ser. 471:37–50 [Google Scholar]
  98. Nielsen LT, Krock B, Hansen PJ. 2013. Production and excretion of okadaic acid, pectenotoxin-2 and a novel dinophysistoxin from the DSP-causing marine dinoflagellate Dinophysis acuta—effects of light, food availability and growth phase. Harmful Algae 23:34–45 [Google Scholar]
  99. Nishitani G, Nagai S, Hayakawa S, Kosaka Y, Sakurada K. et al. 2012. Multiple plastids collected by the dinoflagellate Dinophysis mitra through kleptoplastidy. Appl. Environ. Microbiol. 78:813–21 [Google Scholar]
  100. Olli K, Riser CW, Wassmann P, Ratkova T, Arashkevich E, Pasternak A. 2002. Seasonal variation in vertical flux of biogenic matter in the marginal ice zone and the central Barents Sea. J. Mar. Syst. 38:189–204 [Google Scholar]
  101. Packard TT, Dugdale RC, Goering JJ, Barber RT. 1978. Nitrate reductase-activity in subsurface waters of Peru Current. J. Mar. Res. 36:59–76 [Google Scholar]
  102. Park JS, Myung G, Kim HS, Cho BC, Yih W. 2007. Growth responses of the marine photosynthetic ciliate Myrionecta rubra to different cryptomonad strains. Aquat. Microb. Ecol. 48:83–90 [Google Scholar]
  103. Park MG, Park JS, Kim M, Yih W. 2008. Plastid dynamics during survival of Dinophysis caudata without its ciliate prey. J. Phycol. 44:1154–63 [Google Scholar]
  104. Pawlowski J, Burki F. 2009. Untangling the phylogeny of amoeboid protist. J. Eukaryot. Microbiol. 56:16–25 [Google Scholar]
  105. Pérez MT, Dolan JR, Fukai E. 1997. Planktonic oligotrich ciliates in the NW Mediterranean: growth rates and consumption by copepods. Mar. Ecol. Prog. Ser. 155:89–101 [Google Scholar]
  106. Pitta P, Giannakouru A. 2000. Planktonic ciliates in the oligotrophic Eastern Mediterranean: vertical, spatial distribution and mixotrophy. Mar. Ecol. Prog. Ser. 194:269–82 [Google Scholar]
  107. Putt M. 1990a. Abundance, chlorophyll content and photosynthetic rates of ciliates in the Nordic Seas during summer. Deep-Sea Res. 37:1713–31 [Google Scholar]
  108. Putt M. 1990b. Metabolism of photosynthate in the chloroplast-retaining ciliate Laboea strobila. Mar. Ecol. Prog. Ser. 60:271–81 [Google Scholar]
  109. Rottberger J, Gruber A, Boenigk J, Kroth P. 2013. Influence of nutrients and light on autotrophic, mixotrophic and heterotrophic freshwater chrysophytes. Aquat. Microb. Ecol. 71:179–91 [Google Scholar]
  110. Ryther JH. 1967. Occurrence of red water off Peru. Nature 214:1318–19 [Google Scholar]
  111. Safi KA, Hall JA. 1999. Mixotrophic and heterotrophic nanoflagellate grazing in the convergence zone east of New Zealand. Aquat. Microb. Ecol. 20:83–93 [Google Scholar]
  112. Saito H, Suzuki K, Hinuma A, Ota T, Fukami K. et al. 2005. Responses of microzooplankton to in situ iron fertilization in the western subarctic Pacific (SEEDS). Prog. Oceanogr. 64:223–36 [Google Scholar]
  113. Saiz E, Calbet A. 2011. Copepod feeding in the ocean: scaling patterns, composition of their diet and the bias of estimates due to microzooplankton grazing during incubations. Hydrobiologia 666:181–96 [Google Scholar]
  114. Sanders RW, Berninger U-G, Lim EL, Kemp PF, Caron DA. 2000. Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank. Mar. Ecol. Prog. Ser. 192:103–18 [Google Scholar]
  115. Sanders RW, Gast RJ. 2012. Bacterivory by phototrophic picoplankton and nanoplankton in Arctic waters. FEMS Microbiol. Ecol. 82:242–53 [Google Scholar]
  116. Schoener DM, McManus GB. 2012. Plastid retention, use, and replacement in a kleptoplastidic ciliate. Aquat. Microb. Ecol. 67:177–87 [Google Scholar]
  117. Sellers CG, Gast RJ, Sanders RW. 2014. Selective feeding and foreign plastid retention in an Antarctic dinoflagellate. J. Phycol. 50:1081–88 [Google Scholar]
  118. Siano R, Montresor M, Probert I, Not F, de Vargas C. 2010. Pelagodinium gen. nov. and P. bèii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 161:385–99 [Google Scholar]
  119. Skovgaard A, Hansen PJ, Stoecker DK. 2000. Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. I. Effects of phagotrophy and irradiance on photosynthesis and carbon content. Mar. Ecol. Prog. Ser. 201:129–36 [Google Scholar]
  120. Smalley GW, Coats DW, Stoecker DK. 2003. Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar. Ecol. Prog. Ser. 262:137–51 [Google Scholar]
  121. Smalley GW, Coats DW, Stoecker DK. 2012. Influence of inorganic nutrients, irradiance, and time of day on food uptake by the mixotrophic dinoflagellate Neoceratium furca. Aquat. Microb. Ecol. 68:29–41 [Google Scholar]
  122. Smith M, Hansen PJ. 2007. Interaction between Mesodinium rubrum and its prey: importance of prey concentration, irradiance and pH. Mar. Ecol. Prog. Ser. 338:61–70 [Google Scholar]
  123. Stickney HL, Hood RR, Stoecker DK. 2000. The impact of mixotrophy on planktonic marine ecosystems. Ecol. Model. 125:203–230 [Google Scholar]
  124. Stoecker DK. 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J. Protistol. 34:281–90 [Google Scholar]
  125. Stoecker DK, Johnson MD, de Vargas C, Not F. 2009. Acquired phototrophy in aquatic protists. Aquat. Microb. Ecol. 37:279–310 [Google Scholar]
  126. Stoecker DK, Michaels AE. 1991. Respiration, photosynthesis and carbon metabolism in planktonic ciliates. Mar. Biol. 108:441–47 [Google Scholar]
  127. Stoecker DK, Silver MW, Michaels AE, Davis LH. 1988. Obligate mixotrophy in Laboea strobilia, a ciliate which retains chloroplasts. Mar. Biol. 99:415–23 [Google Scholar]
  128. 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]
  129. Stoecker DK, Swanberg N, Tyler S. 1989. Oceanic mixotrophic flatworms. Mar. Ecol. Prog. Ser. 58:41–51 [Google Scholar]
  130. Stoecker DK, Weigel AC, Stockwell DA, Lomas MW. 2014. Microzooplankton: abundance, biomass and contribution to chlorophyll in the Eastern Bering Sea in summer. Deep-Sea Res. II 109:134–44 [Google Scholar]
  131. Stukel MR, Landry MR, Selph KE. 2011. Nanoplankton mixotrophy in the eastern equatorial Pacific. Deep-Sea Res. II 58:378–86 [Google Scholar]
  132. Sunda WG, Graneli E, Gobler CJ. 2006. Positive feedback and the development and persistence of ecosystem disruptive algal blooms. J. Phycol. 42:963–74 [Google Scholar]
  133. Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M. et al. 2013. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. PNAS 110:11463–68 [Google Scholar]
  134. Swanberg NR. 1983. The trophic role of colonial Radiolaria in oligotrophic oceanic environments. Limnol. Oceanogr. 28:655–66 [Google Scholar]
  135. Swanberg NR, Caron DA. 1991. Patterns of sarcodine feeding in epipelagic oceanic plankton. J. Plankton Res. 13:287–312 [Google Scholar]
  136. Sweeney BM. 1976. Pedinomonas noctilucae (Prasinophyceae), flagellate symbiotic in Noctiluca (Dinophyceae) in Southeast Asia. J. Phycol. 12:460–64 [Google Scholar]
  137. Tarangkoon W, Hansen G, Hansen PJ. 2010. Spatial distribution of symbiont-bearing dinoflagellates in the Indian Ocean in relation to oceanographic regimes. Aquat. Microb. Ecol. 58:197–213 [Google Scholar]
  138. Taylor FJR, Blackbourn DJ, Blackbourn J. 1971. The red-water ciliate Mesodinium rubrum and its “incomplete symbionts”: a review including new ultrastructural observations. J. Fish. Res. Board Can. 28:391–407 [Google Scholar]
  139. Thingstad TF, Havskum H, Garde K, Riemann B. 1996. On the strategy of “eating your competitor”: a mathematical analysis of algal mixotrophy. Ecology 77:2108–18 [Google Scholar]
  140. Tillmann U. 2003. Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum. Aquat. Microb. Ecol. 32:73–84 [Google Scholar]
  141. Tong M, Smith JL, Kulis DM, Anderson DM. 2015. Role of dissolved nitrate and phosphate in isolates of Mesodinium rubrum and toxin-producing Dinophysis acuminata. Aquat. Microb. Ecol. 75:169–85 [Google Scholar]
  142. Unrein F, Gasol JM, Massana R. 2010. Dinobryon faculiferum (Chrysophyta) in coastal Mediterranean seawater: presence and grazing impact on bacteria. J. Plankton Res. 32:559–64 [Google Scholar]
  143. Unrein F, Gasol JM, Not F, Forn I, Massana R. 2014. Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. ISME J. 8:164–76 [Google Scholar]
  144. Unrein F, Massana R, Alonso-Sáez L, Gasol JM. 2007. Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol. Oceanogr. 52:456–69 [Google Scholar]
  145. Våge S, Castellani M, Giske J, Thingstad TJ. 2013. Successful strategies in size structured mixotrophic food webs. Aquat. Ecol. 47:329–47 [Google Scholar]
  146. Wang L, Lin X, Goes JI, Lin S. 2016. Phylogenetic analyses of three genes of Pedinomonas noctilucae, the green endosymbiont of the marine dinoflagellate Noctiluca scintillans, reveal its affiliation to the order Marsupiomonadales (Chlorophyta, Pedinophyceae) under the reinstated name Protoeuglena noctilucae. Protist 167:205–16 [Google Scholar]
  147. Wang Z, O'Shaughnessy TJ, Soto CM, Rahbar AM, Robertson KL. et al. 2012. Function and regulation of Vibrio campbellii proteorhodopsin: acquired phototrophy in a classical organoheterotroph. PLOS ONE 7:e38749 [Google Scholar]
  148. Ward BA, Dutkiewicz S, Barton AD, Follows MJ. 2011. Biophysical aspects of resource acquisition and competition in algal mixotrophs. Am. Nat. 178:98–112 [Google Scholar]
  149. Ward BA, Follows MJ. 2016. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. PNAS 113:2958–63 [Google Scholar]
  150. Weber F, Anderson R, Foissner W, Mylnikov AP, Jürgens K. 2014. Morphological and molecular approaches reveal highly stratified protist communities along Baltic Sea pelagic redox gradients. Aquat. Microb. Ecol. 73:1–16 [Google Scholar]
  151. Wisecaver JH, Hackett JD. 2010. Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genom. 11:366 [Google Scholar]
  152. Zubkov MV, Tarran GA. 2008. High bactivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455:224–26 [Google Scholar]
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