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Hydrobiologia

, Volume 831, Issue 1, pp 5–21 | Cite as

Grazing impact and prey selectivity of picoplanktonic cells by mixotrophic flagellates in oligotrophic lakes

  • Marina Gerea
  • Claudia Queimaliños
  • Fernando UnreinEmail author
PHYTOPLANKTON & BIOTIC INTERACTIONS

Abstract

Mixotrophy by planktonic algae can dominate picoplankton predation in oligotrophic environments. We compared the grazing activity and prey preference of different mixotrophic taxa from natural communities of two oligotrophic shallow lakes (Escondido and Morenito) by performing eight laboratory grazing experiments using three different fluorescent prey (bacteria, picocyanobacteria, and picoeukaryotic algae). Eight taxa of mixotrophic flagellates (MF) corresponding to five different Classes, and two size categories of heterotrophic flagellates were distinguished. Chesson index showed that the ten identified protists preferred picocyanobacteria than bacteria, while picoeukaryotic algae were not ingested by any flagellate. In both lakes, MFs were responsible for ca. 80% of the picoplankton ingestion due to flagellates, and more than 50% of the total grazing impact when considering all flagellates, ciliates, and rotifers. Pseudopedinella spp. (Dictyochophyceae), Chrysochromulina parva (Haptophyceae), and Dinobryon divergens (Chrysophyceae) were the most important predators, while Plagioselmis lacustris (Cryptophyceae) and Chrysophyceae > 5 µm showed the lowest grazing rates. Overall, our findings support the idea of MF being the main picoplankton predators in oligotrophic systems. Besides, we also conclude that herbivory represents a key process in the mixotrophic carbon cycling in oligotrophic environments.

Keywords

Grazing rate Mixotrophy Bacterivory Herbivory Picocyanobacteria Bacteria 

Notes

Acknowledgements

We are grateful to Dr. Miguel Battini for his help in the sampling events and especially to Dr. Carolina Soto Cárdenas for her help with nutrient determinations. We thank Dr. Cristian D. Torres for his assistance in statistical analyses. We also thank the San Carlos de Bariloche Town Council for granting permission to sample lakes within its jurisdiction. We thank Dr. Sylvia Bonilla and Dr. Angela Juárez who kindly provided the strains to prepare the FLPs. This work was supported by the Consejo Superior de Investigaciones Científicas – Consejo Nacional de Investigaciones Científicas y Técnicas (CSIC-CONICET) (Spain-Argentina) Project PROBA (2007 AR0018, CSIC), the Spanish Project MIXANTAR (REN 2002-11396-E/ANT), and by the Argentinean projects CONICET-PIP 01301, FONCYT-PICT 32732, and UNComahue 04/B166. Marina Gerea, Claudia Queimaliños and Fernando Unrein are CONICET researchers.

Supplementary material

10750_2018_3610_MOESM1_ESM.pdf (33 kb)
Supplementary material 1 (PDF 32 kb)

References

  1. APHA, 2005. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, AWWA, Washington, DC.Google Scholar
  2. Alonso, C., V. Rocco, J. P. Barriga, M. Á. Battini & H. Zagarese, 2004. Surface avoidance by freshwater zooplankton: field evidence on the role of ultraviolet radiation. Limnology and Oceanography 49: 225–232.CrossRefGoogle Scholar
  3. Ballen-Segura, M., M. Felip & J. Catalan, 2017. Some mixotrophic flagellate species selectively graze on Archaea. Applied and Environmental Microbiology 83: e02317.CrossRefGoogle Scholar
  4. Bastidas Navarro, M., B. Modenutti, C. Callieri, R. Bertoni & E. Balseiro, 2009. Balance between primary and bacterial production in North Patagonian shallow lakes. Aquatic Ecology 43: 867–878.CrossRefGoogle Scholar
  5. Bertilsson, S., O. Berglund, D. M. Karl & S. W. Chisholm, 2003. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnology and Oceanography 48: 1721–1731.CrossRefGoogle Scholar
  6. Bird, D. F. & J. Kalff, 1986. Bacterial grazing by planktonic lake algae. Science 231: 493–495.CrossRefGoogle Scholar
  7. Bird, D. F. & J. Kalfl, 1987. Algal phagotrophy: regulating factors and importance relative to photosynthesis in Dinobryon (Chrysophyceae). Limnology and Oceanography 32: 277–284.CrossRefGoogle Scholar
  8. Børsheim, K. Y. & G. Bratbak, 1987. Cell volume to cell carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Marine Ecology Progress Series 36: 171–175.CrossRefGoogle Scholar
  9. Burnham, K. P. & D. R. Anderson, 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods and Research 33: 261–304.CrossRefGoogle Scholar
  10. Caron, D. A., R. W. Sanders, E. L. Lim, C. Marrasé, L. A. Amaral, S. Whitney, R. B. Aoki & K. G. Porter, 1993. Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobryon cylindricum. Microbial ecology 25: 93–111.CrossRefGoogle Scholar
  11. Chesson, J., 1983. The estimation and analysis of preference and its relatioship to foraging models. Ecology 64: 1297–1304.CrossRefGoogle Scholar
  12. Chrzanowski, T. H., N. C. Lukomski & J. P. Grover, 2010. Element stoichiometry of a mixotrophic protist grown under varying resource conditions. Journal of Eukaryotic Microbiology 57: 322–327.CrossRefGoogle Scholar
  13. Diaz, M. & F. Pedrozo, 1993. Seasonal succession of phytoplankton in a small Andean patagonian lake (Rep. Argentina) and some considerations about the PEG Model. Archiv fur Hydrobiologie 127: 167–184.Google Scholar
  14. Diaz, M., F. Pedrozo, C. Reynolds & P. Temporetti, 2007. Chemical composition and the nitrogen-regulated trophic state of Patagonian lakes. Limnologica—Ecology and Management of Inland Waters 37: 17–27.CrossRefGoogle Scholar
  15. Domaizon, I., S. Viboud & D. Fontvieille, 2003. Taxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy—importance of mixotrophy. FEMS Microbiology Ecology 46: 317–329.CrossRefGoogle Scholar
  16. Fagerbakke, K. M., M. Heldal & S. Norland, 1996. Content of carbon, nitrogen, oxygen, sulfur and phosphorus in native aquatic and cultured bacteria. Aquatic Microbial Ecology 10: 15–27.CrossRefGoogle Scholar
  17. Fenchel, T., 1982. Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Marine Ecology Progress Series 8: 211–223.CrossRefGoogle Scholar
  18. Flynn, K. J., D. K. Stoecker, A. Mitra, J. A. Raven, P. M. Glibert, P. J. Hansen, E. Graneli & J. M. Burkholder, 2012. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research 35: 3–11.CrossRefGoogle Scholar
  19. Gerea, M., C. Queimalinos, M. R. Schiaffino, I. Izaguirre, I. Forn, R. Massana & F. Unrein, 2013. In situ prey selection of mixotrophic and heterotrophic flagellates in Antarctic oligotrophic lakes: an analysis of the digestive vacuole content. Journal of Plankton Research 35: 201–212.CrossRefGoogle Scholar
  20. Gerea, M., J. Saad, I. Izaguirre, C. Queimaliños, J. Gasol & F. Unrein, 2016. Presence, abundance and bacterivory impact of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments. Aquatic Microbial Ecology 76: 219–232.CrossRefGoogle Scholar
  21. Gerea, M., G. L. Pérez, F. Unrein, C. Soto Cárdenas, D. Morris & C. Queimaliños, 2017. CDOM and the underwater light climate in two shallow North Patagonian lakes: evaluating the effects on nano and microphytoplankton community structure. Aquatic Sciences 79: 231–248.CrossRefGoogle Scholar
  22. Hansen, P. J. & M. Hjorth, 2002. Growth and grazing responses of Chrysochromulina ericina (Prymnesiophyceae): the role of irradiance, prey concentration and pH. Marine Biology 141: 975–983.CrossRefGoogle Scholar
  23. Hitchman, R. B. & H. L. J. Jones, 2000. The role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial pond. Freshwater Biology 43: 231–241.CrossRefGoogle Scholar
  24. Isaksson, A., A. Bergström, P. Blomqvist & M. Jansson, 1999. Bacterial grazing by phagotrophic phytoflagellates in a deep humic lake in northern Sweden. Journal of Plankton Research 21: 247–268.CrossRefGoogle Scholar
  25. Izaguirre, I., R. Sinistro, M. Schiaffino, M. Sánchez, F. Unrein & R. Massana, 2012. Grazing rates of protists in wetlands under contrasting light conditions due to floating plants. Aquatic Microbial Ecology 65: 221–232.CrossRefGoogle Scholar
  26. Jansson, M., P. Blomqvist, A. Jonsson & A. K. Bergström, 1996. Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket. Limnology and Oceanography 41: 1552–1559.CrossRefGoogle Scholar
  27. Jones, R. I., 1994. Mixotrophy in planktonic protist as a spectrum of nutritional strategies. Marine Microbial Food Webs 8: 87–96.Google Scholar
  28. Jones, H., 1997. A classification of mixotrophic protists based on their behaviour. Freshwater Biology 37: 35–43.CrossRefGoogle Scholar
  29. Jones, R. I., 2000. Mixotrophy in planktonic protists: an overview. Freshwater Biology 45: 219–226.CrossRefGoogle Scholar
  30. Jones, R. I. & S. Rees, 1994a. Characteristics of particle uptake by the phagotrophic phytoflagellate Dinobryon divergens. Marine Microbial Food Webs 8: 97–110.Google Scholar
  31. Jones, R. I. & S. Rees, 1994b. Influence of temperature and light on particle ingestion by the freshwater phytoplankton Dinobryon. Archiv fur Hydrobiologie 132: 203–211.Google Scholar
  32. Jones, H. L. J., B. S. C. Leadbeater & J. C. Green, 1993. Mixotrophy in marine species of Chrysochromulina (Prymnesiophyceae): ingestion and digestion of a small green flagellate. Journal of the Marine Biological Association of the UK 73: 283–296.CrossRefGoogle Scholar
  33. Jürgens, K. & W. DeMontt, 1995. Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnology and Oceanography 40: 1503–1507.CrossRefGoogle Scholar
  34. Jürgens, K. & C. Matz, 2002. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie van Leeuwenhoek 81: 413–434.CrossRefGoogle Scholar
  35. Kamjunke, N., T. Henrichs & U. Gaedke, 2007. Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re-oligotrophication. Journal of Plankton Research 29: 39–46.CrossRefGoogle Scholar
  36. Kiørboe, T., H. P. Grossart, H. Ploug, K. Tang & B. Auer, 2004. Particle-associated flagellates: swimming patterns, colonization rates, and grazing on attached bacteria. Aquatic Microbial Ecology 35: 141–152.CrossRefGoogle Scholar
  37. Massana, R., J. Gasol, P. K. Bjornsen, N. Black, A. Hagström, S. Hietanen, B. Hygum, J. Kuparinen & C. Pedrós-alió, 1997. Measurement of bacterial size via image analysis of epifluorescence preparations: description of an inexpensive system and solutions to some of the most common problems. Scientia Marina 61: 397–407.Google Scholar
  38. McKie-Krisberg, Z. M., R. J. Gast & R. W. Sanders, 2014. Physiological responses of three species of Antarctic mixotrophic phytoflagellates to changes in light and dissolved nutrients. Microbial Ecology 70: 21–29.CrossRefGoogle Scholar
  39. McKie-Krisberg, Z. M. & R. W. Sanders, 2014. Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans. The ISME journal 8: 1953–1961.CrossRefGoogle Scholar
  40. Medina-Sánchez, J. M., M. Villar-Argaiz & P. Carrillo, 2004. Neither with nor without you: a complex algal control on bacterioplankton in a high mountain lake. Limnology and Oceanography 49: 1722–1733.CrossRefGoogle Scholar
  41. Menden-Deuer, S. & E. J. Lessard, 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45: 569–579.CrossRefGoogle Scholar
  42. Millette, N. C., J. J. Pierson, A. Aceves & D. K. Stoecker, 2016. Mixotrophy in Heterocapsa rotundata: a mechanism for dominating the winter phytoplankton. Limnology and Oceanography 62: 836–845.CrossRefGoogle Scholar
  43. Mitra, A., K. J. Flynn, J. M. Burkholder, T. Berge, A. Calbet, J. A. Raven, E. Granéli, P. M. Glibert, P. J. Hansen, D. K. Stoecker, F. Thingstad, U. Tillmann, S. Våge, S. Wilken & M. V. Zubkov, 2014. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11: 995–1005.CrossRefGoogle Scholar
  44. Mitra, A., K. J. Flynn, U. Tillmann, J. A. Raven, D. Caron, D. K. Stoecker, F. Not, P. J. Hansen, G. Hallegraeff, R. Sanders, S. Wilken, G. McManus, M. Johnson, P. Pitta, S. Våge, T. Berge, A. Calbet, F. Thingstad, H. J. Jeong, J. Burkholder, P. M. Glibert, E. Granéli & V. Lundgren, 2016. Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: incorporation of diverse mixotrophic strategies. Protist 167: 106–120.CrossRefGoogle Scholar
  45. Morris, D. P., H. Zagarese, C. E. Williamson, E. G. Balseiro, R. Hargreaves, B. Modenutti, R. Moeller & C. Queimalinos, 1995. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography 40: 1381–1391.CrossRefGoogle Scholar
  46. Norland, S., 1993. The relationship between biomass and volume of bacteria. In Kemp, P. F., B. F. Sherr, E. B. Sherr & J. J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton: 303–307.Google Scholar
  47. Nusch, E. A., 1980. Comparison of different methods for chlorophyll- and phaeopigments determination. Archives Hydrobiology Beih Ergebn Limnology 14: 14–36.Google Scholar
  48. Nygaard, K. & A. Tobiesen, 1993. Bacterivory in algae: a survival strategy during nutrient limitation. Limnology and Oceanography 38: 273–279.CrossRefGoogle Scholar
  49. Pachiadaki, M. G., C. Taylor, A. Oikonomou, M. M. Yakimov, T. Stoeck & V. Edgcomb, 2016. In situ grazing experiments apply new technology to gain insights into deep-sea microbial food webs. Deep-Sea Research Part II: Topical Studies in Oceanography Elsevier 129: 223–231.CrossRefGoogle Scholar
  50. Palsson, C. & W. Granéli, 2004. Nutrient limitation of autotrophic and mixotrophic phytoplankton in a temperate and tropical humic lake gradient. Journal of Plankton Research 26: 1005–1014.CrossRefGoogle Scholar
  51. Pérez, G. L., A. Torremorell, J. Bustingorry, R. Escaray, P. Pérez, M. Diéguez & H. Zagarese, 2010. Optical characteristics of shallow lakes from the Pampa and Patagonia regions of Argentina. Limnologica 40: 30–39.CrossRefGoogle Scholar
  52. Pernthaler, J., K. Šimek, B. Sattler, A. Schwarzenbacher, J. Bobkova & R. Psenner, 1996. Short-term changes of protozoan control on autotrophic picoplankton in an oligo-mesotrophic lake. Journal of Plankton Research 18: 443–462.CrossRefGoogle Scholar
  53. Pernthaler, J., T. Posch, K. Šimek, J. Vrba, R. Amann & R. Psenner, 1997. Contrasting bacterial strategies to coexist with a flagellate predator in an experimental microbial assemblage. Applied and Environmental Microbiology 63: 596–601.PubMedPubMedCentralGoogle Scholar
  54. Pfandl, K., T. Posch & J. Boenigkh, 2004. Unexpected effects of prey dimensions and morphologies on the size selective feeding by two bacterivorous flagellates. Journal of Eukaryotic Microbiology 51: 626–633.CrossRefGoogle Scholar
  55. Porter, K. G. & Y. Feig, 1980. The use of DAPI for identifying aquatic microflora. Limnology and Oceanography 25: 943–948.CrossRefGoogle Scholar
  56. Ptacnik, R., A. Gomes, S. J. Royer, S. A. Berger, A. Calbet, J. C. Nejstgaard, J. M. Gasol, S. Isari, S. D. Moorthi, R. Ptacnikova, M. Striebel, A. F. Sazhin, T. M. Tsagaraki, S. Zervoudaki, K. Altoja, P. D. Dimitriou, P. Laas, A. Gazihan, R. A. Martínez, S. Schabhüttl, I. Santi, D. Sousoni & P. Pitta, 2016. A light-induced shortcut in the planktonic microbial loop. Scientific Reports 6: 1–10.CrossRefGoogle Scholar
  57. Queimaliños, C., 2002. The role of phytoplanktonic size fractions in the microbial food webs in two north Patagonian lakes (Argentina). Archiv fur Hydrobiologie 28: 1236–1240.Google Scholar
  58. Queimaliños, C. & M. Diaz, 2014. Phytoplankton of Andean Patagonian lakes. In Tell, G., I. Izaguirre & H. Pizarro (eds), Freshwater phytoplankton of Argentina 235–256.Google Scholar
  59. Queimaliños, C., M. Reissig, M. D. C. Diéguez, M. Arcagni, S. Ribeiro Guevara, L. Campbell, C. Soto Cárdenas, R. Rapacioli & M. Arribére, 2012. Influence of precipitation, landscape and hydrogeomorphic lake features on pelagic allochthonous indicators in two connected ultraoligotrophic lakes of North Patagonia. The Science of the Total Environment 427–428: 219–228.CrossRefGoogle Scholar
  60. Salat, J. & C. Marrasé, 1994. Exponential and linear estimations of grazing on bacteria: effects of changes in the proportion of marked cells. Marine Ecology Progress Series 104: 205–209.CrossRefGoogle Scholar
  61. Sanders, R. W., 1991. Mixotrophic protists in marine and freshwater ecosystems. Journal of Protozoology 38: 76–81.CrossRefGoogle Scholar
  62. Sanders, R. W., K. G. Porter, S. J. Bennett & A. E. Debiase, 1989. Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnology and Oceanography 34: 673–687.CrossRefGoogle Scholar
  63. Schmidtke, A., E. M. Bell & G. Weithoff, 2006. Potential grazing impact of the mixotrophic flagellate Ochromonas sp. (Chrysophyceae) on bacteria in an extremely acidic lake. Journal of Plankton Research 28: 991–1001.CrossRefGoogle Scholar
  64. Shannon, S. P., 2006. Comparison of Ingestion and Digestion Rates of Ochromonas danica Grazing on Pseudomonas fluorescens of Varying Food Quality. University of Texas at Arlington.Google Scholar
  65. Shannon, S. P., T. H. Chrzanowski & J. P. Grover, 2007. Prey food quality affects flagellate ingestion rates. Microbial ecology 53: 66–73.CrossRefGoogle Scholar
  66. Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81: 293–308.CrossRefGoogle Scholar
  67. Šimek, K., J. Vrba, J. Pernthaler, T. Posch, P. Hartman, J. Nedoma & R. Psenner, 1997. Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Applied and environmental microbiology 63: 587–595.PubMedPubMedCentralGoogle Scholar
  68. Simon, M. & F. Azam, 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Marine Ecology Progress Series 51: 201–213.CrossRefGoogle Scholar
  69. Smalley, G. W., D. W. Coats & D. K. Stoecker, 2003. Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Marine Ecology Progress Series 262: 137–151.CrossRefGoogle Scholar
  70. Soto Cárdenas, C., M. Gerea, P. E. Garcia, G. L. Pérez, M. C. Diéguez, R. Rapacioli, M. Reissig & C. Queimaliños, 2017. Interplay between climate and hydrogeomorphic features and their effect on the seasonal variation of dissolved organic matter in shallow temperate lakes of the Southern Andes (Patagonia, Argentina): a field study based on optical properties. Ecohydrology.  https://doi.org/10.1002/eco.1872.CrossRefGoogle Scholar
  71. Stoecker, D. K., 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. European Journal of Protistology 34: 281–290.CrossRefGoogle Scholar
  72. Strom, S., K. Bright, K. Fredrickson & B. Brahamsha, 2017. The Synechococcus cell surface protein SwmA increases vulnerability to predation by flagellates and ciliates. Limnology and Oceanography 62: 784–794.CrossRefGoogle Scholar
  73. Sun, J. & D. Liu, 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25: 1331–1346.CrossRefGoogle Scholar
  74. Tarbe, A.-L., F. Unrein, S. Stenuite, S. Pirlot, H. Sarmento, D. Sinyinza & J.-P. Descy, 2011. Protist herbivory: a key pathway in the pelagic food web of Lake Tanganyika. Microbial Ecology 62: 314–323.CrossRefGoogle Scholar
  75. Tranvik, L. J., K. G. Porter & J. M. Sieburth, 1989. Occurrence of bacterivory in Cryptomonas, a common freshwater phytoplankter. Oecologia 78: 473–476.CrossRefGoogle Scholar
  76. Unrein, F., J. M. Gasol & R. Massana, 2010. Dinobryon faculiferum (Chrysophyta) in coastal Mediterranean seawater: presence and grazing impact on bacteria. Journal of Plankton Research 32: 559–564.CrossRefGoogle Scholar
  77. Unrein, F., J. M. Gasol, F. Not, I. Forn & R. Massana, 2014. Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. The ISME Journal 8: 164–176.CrossRefGoogle Scholar
  78. Unrein, F., R. Massana, L. Alonso-Sáez & J. M. Gasol, 2007. Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnology and Oceanography 52: 456–469.CrossRefGoogle Scholar
  79. Urabe, J., T. B. Gurung, T. Yoshida, T. Sekino, M. Nakanishi, M. Maruo & E. Nakayama, 2000. Diel changes in phagotrophy by Cryptomonas in Lake Biwa. Limnology and Oceanography 45: 1558–1563.CrossRefGoogle Scholar
  80. Vadstein, O., 2000. Heterotrophic, planktonic bacteria and cycling of phosphorus. In Schink, B. (ed), Advances in Microbial Ecology 2000.Google Scholar
  81. Vazquez-Dominguez, E., F. Peters, J. Gasol & D. Vaqué, 1999. Measuring the grazing losses of picoplankton: methodological improvements in the use of fluorescently labeled tracers combined with flow cytometry. Aquatic Microbial Ecology 20: 119–128.CrossRefGoogle Scholar
  82. Worden, A. Z., G. Drive, L. Jolla & J. K. Nolan, 2004. Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnology and Oceanography 49: 168–179.CrossRefGoogle Scholar
  83. Zhang, X. & M. M. Watanabe, 2001. Grazing and growth of the mixotrophic chrysomonad Poterioochromonas malhamensis (Chrysophyceae) feeding on algae. Journal of Phycology 37: 738–743.CrossRefGoogle Scholar
  84. Zubkov, M. V. & G. A. Tarran, 2008. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224–226.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Grupo de Ecología de Sistemas Acuáticos a escala de Paisaje (GESAP), INIBIOMACONICET-Universidad Nacional del ComahueBarilocheArgentina
  2. 2.Laboratorio de Ecología y Fotobiología Acuática, IIB-INTECHUNSAM-CONICETChascomúsArgentina
  3. 3.Consejo Nacional de Investigación Científica y Técnica (CONICET)Buenos AiresArgentina

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