Skip to main content
SpringerLink
Log in

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

  • PHYTOPLANKTON & BIOTIC INTERACTIONS
  • Published:
Hydrobiologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • APHA, 2005. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, AWWA, Washington, DC.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Ballen-Segura, M., M. Felip & J. Catalan, 2017. Some mixotrophic flagellate species selectively graze on Archaea. Applied and Environmental Microbiology 83: e02317.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bird, D. F. & J. Kalff, 1986. Bacterial grazing by planktonic lake algae. Science 231: 493–495.

    Article  CAS  Google Scholar 

  • Bird, D. F. & J. Kalfl, 1987. Algal phagotrophy: regulating factors and importance relative to photosynthesis in Dinobryon (Chrysophyceae). Limnology and Oceanography 32: 277–284.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods and Research 33: 261–304.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Chesson, J., 1983. The estimation and analysis of preference and its relatioship to foraging models. Ecology 64: 1297–1304.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Fenchel, T., 1982. Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Marine Ecology Progress Series 8: 211–223.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Jones, R. I., 1994. Mixotrophy in planktonic protist as a spectrum of nutritional strategies. Marine Microbial Food Webs 8: 87–96.

    Google Scholar 

  • Jones, H., 1997. A classification of mixotrophic protists based on their behaviour. Freshwater Biology 37: 35–43.

    Article  Google Scholar 

  • Jones, R. I., 2000. Mixotrophy in planktonic protists: an overview. Freshwater Biology 45: 219–226.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • Jürgens, K. & W. DeMontt, 1995. Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnology and Oceanography 40: 1503–1507.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Menden-Deuer, S. & E. J. Lessard, 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45: 569–579.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Nusch, E. A., 1980. Comparison of different methods for chlorophyll- and phaeopigments determination. Archives Hydrobiology Beih Ergebn Limnology 14: 14–36.

    CAS  Google Scholar 

  • Nygaard, K. & A. Tobiesen, 1993. Bacterivory in algae: a survival strategy during nutrient limitation. Limnology and Oceanography 38: 273–279.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Porter, K. G. & Y. Feig, 1980. The use of DAPI for identifying aquatic microflora. Limnology and Oceanography 25: 943–948.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Queimaliños, C. & M. Diaz, 2014. Phytoplankton of Andean Patagonian lakes. In Tell, G., I. Izaguirre & H. Pizarro (eds), Freshwater phytoplankton of Argentina 235–256.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Sanders, R. W., 1991. Mixotrophic protists in marine and freshwater ecosystems. Journal of Protozoology 38: 76–81.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • Shannon, S. P., T. H. Chrzanowski & J. P. Grover, 2007. Prey food quality affects flagellate ingestion rates. Microbial ecology 53: 66–73.

    Article  Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81: 293–308.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Simon, M. & F. Azam, 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Marine Ecology Progress Series 51: 201–213.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Stoecker, D. K., 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. European Journal of Protistology 34: 281–290.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Sun, J. & D. Liu, 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25: 1331–1346.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Tranvik, L. J., K. G. Porter & J. M. Sieburth, 1989. Occurrence of bacterivory in Cryptomonas, a common freshwater phytoplankter. Oecologia 78: 473–476.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Vadstein, O., 2000. Heterotrophic, planktonic bacteria and cycling of phosphorus. In Schink, B. (ed), Advances in Microbial Ecology 2000.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Zubkov, M. V. & G. A. Tarran, 2008. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224–226.

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Grupo de Ecología de Sistemas Acuáticos a escala de Paisaje (GESAP), INIBIOMA, CONICET-Universidad Nacional del Comahue, Quintral 1250, R8400FRD, Bariloche, Rio Negro, Argentina

    Marina Gerea & Claudia Queimaliños

  2. Laboratorio de Ecología y Fotobiología Acuática, IIB-INTECH, UNSAM-CONICET, Chascomús, Buenos Aires, Argentina

    Fernando Unrein

  3. Consejo Nacional de Investigación Científica y Técnica (CONICET), Buenos Aires, Argentina

    Marina Gerea, Claudia Queimaliños & Fernando Unrein

Authors
  1. Marina Gerea
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Queimaliños
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Unrein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernando Unrein.

Additional information

Guest editors: Hugo Sarmento, Irina Izaguirre, Vanessa Becker & Vera L. M. Huszar / Phytoplankton and its Biotic Interactions

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gerea, M., Queimaliños, C. & Unrein, F. Grazing impact and prey selectivity of picoplanktonic cells by mixotrophic flagellates in oligotrophic lakes. Hydrobiologia 831, 5–21 (2019). https://doi.org/10.1007/s10750-018-3610-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3610-3

Keywords

Search

Navigation