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Hydrobiologia

, Volume 831, Issue 1, pp 55–70 | Cite as

Plankton community interactions in an Amazonian floodplain lake, from bacteria to zooplankton

  • I. B. Feitosa
  • V. L. M. HuszarEmail author
  • C. D. Domingues
  • E. Appel
  • R. Paranhos
  • R. M. Almeida
  • C. W. C. Branco
  • W. R. Bastos
  • H. Sarmento
PHYTOPLANKTON & BIOTIC INTERACTIONS

Abstract

The simple view of the classical phytoplankton–zooplankton–fish food chain (CFC) has been replaced by a more complex framework, integrating microbial compartments (microbial food web, MFW). Few studies considered all components of the pelagic MFW in freshwaters and mostly are from temperate regions. We investigated carbon partitioning in the CFC and the MFW in an Amazonian floodplain system and analyzed the strength of interactions among components through structure equation modeling. We hypothesized that (i) MFW contributes highly to total plankton biomass throughout the year; and (ii) all plankton communities increase in biomass during low water, increasing the role of trophic interactions. We collected 30 subsurface samples (nutrients and plankton communities). MFW predominated over CFC in carbon biomass, and plankton components and their interactions changed according to the contrasting water level. Because phosphorus can be a potentially limiting resource for strict primary producers, higher biomass and a more complex MFW occurred during low water. We concluded that hydrology is a key factor shaping biotic interactions during low-water periods, and that MFW plays a key role in floodplain lakes, being potential mixotrophy an important strategy for phytoplankton.

Keywords

Microbial food web Classical food chain Seasonal interactions Mixotrophy Structural equation modeling 

Notes

Acknowledgements

We express our gratitude to Raimundo and Rongelina for providing access to the lake and sometimes much more. We thank Janet W. Reid (JWR Associates) for revising the English text. This research was financially supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil CNPq (Grant 552331/2011-2). VH was partially supported by CNPq (Grant 304284/2017-3). HS’s work was supported by CNPq (Grant 309514/2017-7) and by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Grant 2014/13139-3). We would also like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a Master’s scholarship for IF.

Supplementary material

10750_2018_3855_MOESM1_ESM.docx (185 kb)
Supplementary material 1 (DOCX 184 kb)

References

  1. Almeida, R. M., F. Roland, S. J. Cardoso, V. F. Farjalla, R. L. Bozelli & N. O. Barros, 2015a. Viruses and bacteria in floodplain lakes along a major Amazon tributary respond to distance to the Amazon River. Frontiers in Microbiology 6: 158.PubMedPubMedCentralGoogle Scholar
  2. Almeida, R. M., L. Tranvik, V. L. M. Huszar, S. Sobek, R. Mendonça, N. Barros, G. Boemer Jr., J. D. Arantes & F. Roland, 2015b. Phosphorus transport by the largest Amazon tributary (Madeira River, Brazil) and its sensitivity to precipitation and damming. Inland Waters 5: 275–282.Google Scholar
  3. Alvares, C. A., J. L. Stape, P. C. Sentelhas, J. L. M. Gonçalves & G. Sparovek, 2014. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711–728.Google Scholar
  4. Amaral, J. H. F., A. V. Borges, J. M. Melack, H. Sarmento, P. M. Barbosa, D. Kasper, M. L. de Melo, D. De Fex-Wolf, J. S. da Silva & B. R. Forsberg, 2018. Influence of plankton metabolism and mixing depth on CO2 dynamics in an Amazon floodplain lake. Science of the Total Environment 630: 1381–1393.PubMedGoogle Scholar
  5. ANA – Agência Nacional de Águas, [available on internet at www.ana.gov.br/telemetria], station 15630000, Humaitá, Amazonas State.
  6. Anésio, A. M., P. C. Abreu & F. A. Esteves, 1997. Influence of the hydrological cycle on the bacterioplankton of an impacted clear water Amazonian Lake. Microbial Ecology 34: 66–73.PubMedGoogle Scholar
  7. Aoyagui, A. S. M. & C. C. Bonecker, 2004. Rotifers in different environments of the Upper Paraná River floodplain (Brazil): richness, abundance and the relationship with the connectivity. Hydrobiologia 522: 281–290.Google Scholar
  8. Atwood, T. B., E. Hammill, H. S. Greig, P. Kratina, J. B. Shurin, D. S. Srivastava & J. S. Richardson, 2013. Predator-induced reduction of freshwater carbon dioxide emissions. Nature Geoscience 6: 191–194.Google Scholar
  9. Auer, B., U. Elzer & H. Arndt, 2004. Comparison of pelagic food webs in lakes along a trophic gradient and with seasonal aspects: influence of resource and predation. Journal of Plankton Research 26: 697–709.Google Scholar
  10. Aufdenkampe, A. K., E. Mayorga, P. A. Raymond, et al., 2011. Riverine coupling of biogeochemical cycles between land, oceans, and atmosphere. Frontiers in Ecology and Environment 9: 53–60.Google Scholar
  11. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10: 257–263.Google Scholar
  12. Barros, N., V. F. Farjalla, M. C. Soares, R. C. N. Melo & F. Roland, 2010. Virus-Bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian Floodplain Lake. Applied and Environmental Microbiology 76: 7194–7201.PubMedPubMedCentralGoogle Scholar
  13. Bates, D., M. Machler, B. M. Bolker & S. C. Walker, 2015. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 67: 1–48.Google Scholar
  14. Berninger, U.-G., B. J. Finlay & P. Kuuppo-Leinikki, 1991. Protozoan control of bacterial abundances in freshwater. Limnology and Oceanography 36: 139–147.Google Scholar
  15. Bolker, B. M., M. E. Brooks, C. J. Clark, S. W. Geange, J. R. Poulsen, M. H. H. Stevens & S. W. Jada-Simone, 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24: 127–135.Google Scholar
  16. Bollen, K. A. & R. A. Stine, 1992. Bootstrapping goodness-of-fit measures in structural equation models. Sociological Methods & Research 21: 205–229.Google Scholar
  17. Borsheim, 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.Google Scholar
  18. Bozelli, R. L., 1994. Zooplankton community density in relation to water fluctuation and inorganic turbidity in an Amazonian lake, Lago Batata, State of Pará, Brazil. Amazoniana 13: 17–32.Google Scholar
  19. Burns, C. W. & L. M. Galbraith, 2007. Relating planktonic microbial food web structure in lentic freshwater ecosystems to water quality and land use. Journal of Plankton Research 29: 127–139.Google Scholar
  20. Callieri, C. & J. Stockner, 2002. Freshwater autotrophic picoplankton: a review. Journal of Limnology 61: 1–14.Google Scholar
  21. Callieri, C., A. Pugnett & M. Manca, 1999. Carbon partitioning in the food web of a high mountain lake: from bacteria to zooplankton. Journal of Limnology 58: 144–151.Google Scholar
  22. Carpenter, S. R. & J. F. Kitchell, 1993. The Trophic Cascade in Lakes. Cambridge University Press, Cambridge.Google Scholar
  23. Carvalho, P., S. M. Thomaz & L. M. Bini, 2003. Effects of water level, abiotic and biotic factors on bacterioplankton abundance in lagoons of a tropical floodplain (Paraná River, Brazil). Hydrobiologia 510: 67–74.Google Scholar
  24. Chase, E. M. & F. L. Sayles, 1980. Phosphorus in suspended sediments of the Amazon River. Estuarine and Coastal Marine Science 2: 383–391.Google Scholar
  25. Cole, G. A., 1994. Textbook of Limnology. Waveland Press Inc., Long Grove.Google Scholar
  26. Conty, A. & E. Becares, 2013. Unimodal patterns of microbial communities with eutrophication in Mediterranean shallow lakes. Hydrobiologia 700: 257–265.Google Scholar
  27. Cremona, F., T. Kõiv, V. Kisand, A. Laas, P. Zingel, H. Agasild, T. Feldmann, A. Järvalt, P. Nõges & T. Nõges, 2014. From bacteria to piscivorous fish: estimates of whole-lake and component-specific metabolism with an ecosystem approach. PLoS ONE 9: e101845.PubMedPubMedCentralGoogle Scholar
  28. Crumpton, W. G., T. M. Isenhart & P. D. Mitchell, 1992. Nitrate and organic N analyses with second-derivative spectroscopy. Limnology and Oceanography 37: 907–913.Google Scholar
  29. Domingues, C. D., L. H. S. Silva, L. M. Rangel, L. de Magalhães, R. A. Melo, L. M. Lobão, R. Paiva, F. Roland & H. Sarmento, 2016. Microbial food-web drivers in tropical reservoirs. Microbial Ecology 73: 505–520.PubMedGoogle Scholar
  30. Drakare, S., P. Blomqvist, A. Bergstrom & M. Jansson, 2002. Primary production and phytoplankton in relation to DOC input and bacterioplankton production in humic Lake Örträsket. Freshwater Biology 47: 41–52.Google Scholar
  31. Doherty, M., P. L. Yager, M. A. Moran, V. J. Coles, C. S. Fortunato, A. V. Krusche & B. C. Crump, 2017. Bacterial biogeography across the Amazon River-Ocean Continuum. Frontiers in Microbiology 8: 882.PubMedPubMedCentralGoogle Scholar
  32. Engle, D. L. & O. Sarnelle, 1990. Algal use of sedimentary phosphorus from an Amazon floodplain lake: implications for total phosphorus analysis in turbid waters. Limnology and Oceanography 35: 483–490.Google Scholar
  33. Esquivel, A., A. Barani, M. Macek, R. Soto-Casto & C. Bulit, 2016. The trophic role and impact of plankton ciliates in the microbial web structure of a tropical polymictic lake dominated by filamentous cyanobacteria. Journal of Limnology 75: 93–106.Google Scholar
  34. Fenchel, T., 2008. The microbial loop – 25 years later. Journal of Experimental Marine Biology and Ecology 366: 99–103.Google Scholar
  35. Fermani, P., N. Diovisalvi, A. Torremorell, L. Lagomarsino, H. E. Zagarese & F. Unrein, 2013. The MFW structure of a hypertrophic warm-temperate shallow lake, as affected by contrasting zooplankton assemblages. Hydrobiologia 714: 115–130.Google Scholar
  36. Fernando, C., 1994. Zooplankton, fish and fisheries in tropical freshwaters. Hydrobiologia 272: 105–123.Google Scholar
  37. Flynn, K. J., D. K. Stoecker, A. Mitra, J. A. Raven, P. M. Glibert, P. H. Hansen, E. Granéli & J. M. Burkholder, 2013. Misuse of the phytoplankton–zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research 35: 3–11.Google Scholar
  38. Forsberg, B. R., A. H. Devol, J. E. Richey, L. A. Martinelli & H. dos Santos, 1988. Factors controlling nutrient concentrations in Amazon floodplain lakes. Limnology and Oceanography 33: 41–56.Google Scholar
  39. Forsberg, B. R., J. M. Melack, J. E. Richey & T. P. Pimentel, 2017. Regional and seasonal variability in planktonic photosynthesis and planktonic community respiration in Amazon floodplain lakes. Hydrobiologia 800: 187–206.Google Scholar
  40. Galbraith, L. M. & C. W. Burns, 2010. Drivers of ciliate and phytoplankton community structure across a range of water bodies in southern New Zealand. Journal of Plankton Research 32: 327–339.Google Scholar
  41. Gasol, J. M., C. Pedrós-Alió & D. Vaqué, 2002. Regulation of bacterial assemblages in oligotrophic plankton systems: results from experimental and empirical approaches. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 81: 435–452.Google Scholar
  42. Hambright, K. D., T. Zohary & H. Güde, 2007. Microzooplankton dominate carbon flow and nutrient cycling in a warm subtropical freshwater lake. Limnology and Oceanography 52: 1018–1025.Google Scholar
  43. Hillebrand, H., C. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.Google Scholar
  44. Hu, L. & P. M. Bentler, 1999. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal 6: 1–55.Google Scholar
  45. Huszar, V. L. M. & C. S. Reynolds, 1997. Phytoplankton periodicity and sequences of dominance in an Amazonian flood-plain lake (Lago Batata, Pará, Brasil): responses to gradual environmental change. Hydrobiologia 346: 169–181.Google Scholar
  46. Jeppesen, E., M. Søndergaard, J. P. Jensen, E. Mortensen & O. Sortkjær, 1996. Fish-induced changes in zooplankton grazing on phytoplankton and bacterioplankton: a long-term study in shallow hypertrophic Lake Søbygaard. Journal of Plankton Research 18: 1605–1625.Google Scholar
  47. Jeppesen, E., M. Søndergaard, J. P. Jensen, et al., 2005. Lake responses to reduced nutrient loading - an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.Google Scholar
  48. Junk, W. J., P. B. Bayley & R. E. Sparks, 1989. The flood pulse concept in river flood-plain systems. In Dodge, D. P. (ed.), Proceedings of the International Large Rivers Symposium, Canadian Special Publications in Fisheries and Aquatic Science. NSC Research Press, Ottawa: 110–127.Google Scholar
  49. Junk, W. J., M. T. F. Piedade, J. Schöngart, M. C. Haft & M. Adeney, 2011. A classification of major naturally-occurring Amazonian Lowland Wetlands. Wetlands 31: 623–640.Google Scholar
  50. Karus, K., T. Paaver, H. Agasild & P. Zingel, 2014. The effects of predation by planktivorous juvenile fish on the MFW. European Journal of Protistology 50: 109–121.PubMedGoogle Scholar
  51. Latja, R. & K. Salonen, 1978. Carbon analysis for the determination of individual biomass of planktonic animals. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen 20: 2556–2560.Google Scholar
  52. Leander, B. S., G. Lax, A. Karnkowska, & A. G. B. Simpson, 2017. Euglenida. In Archibald, J. M., Simpson, A. G. B. & C. Slamovits (eds), Handbook of the Protists (2nd edition of the Handbook of Protoctista by Margulis et al.), Springer-Verlag, 39 pp.Google Scholar
  53. Loverde-Oliveira, S. M., V. L. M. Huszar, N. Mazzeo & M. Scheffer, 2009. Hydrology-driven regime shifts in a shallow tropical lake. Ecosystems 12: 807–819.Google Scholar
  54. Lund, J., C. Kipling & E. LeCren, 1958. The inverted microscope method of estimating algal number and the statistical basis of estimation by count. Hydrobiologia 11: 143–170.Google Scholar
  55. Mackereth, F. J. H., J. Heron & J. P. Talling, 1978. Water Analysis. FBA Scientific Publication No, 36.Google Scholar
  56. Manca, M. & P. Comoli, 1999. Studies on zooplankton of Lago Paione Superiore. Journal of Limnology 58: 131–135.Google Scholar
  57. Meira, B. R., F. M. Lansac-Tôha, B. T. Segóvia, P. R. B. Buosi, F. A. Lansac-Tôha & L. F. M. Velho, 2018. The importance of herbivory by protists in lakes of a tropical floodplain system. Aquatic Ecology 52(2–3): 193–210.Google Scholar
  58. Menezes, J. M., 2010. Carbono em lagos amazônicos: conceitos gerais de caso (pCO2 e metabolismo aquático em um lago de águas brancas e um lago de águas pretas). Master’s Dissertation, UFRJ, 66 pp.Google Scholar
  59. Morana, C., H. Sarmento, J.-P. Descy, J. M. Gasol, A. V. Borges, S. Bouillon & F. Darchambeau, 2014. Production of dissolved organic matter by phytoplankton and its uptake by heterotrophic prokaryotes in large tropical lakes. Limnology and Oceanography 59: 1364–1375.Google Scholar
  60. Moreira-Turcq, P., M. P. Bonnet, M. Amorim, M. Bernardes, C. Lagane, L. Maurice & P. Seyler, 2013. Seasonal variability in concentration, composition, age, and fluxes of particulate organic carbon exchanged between the floodplain and Amazon River. Global Biogeochemical Cycles 27: 119–130.Google Scholar
  61. Müller, H. & W. Geller, 1993. Maximum growth rates of aquatic ciliated protozoa: the dependence on body size and temperature reconsidered. Archiv für Hydrobiologie 126: 315–327.Google Scholar
  62. Müller-Navarra, D. C., 2008. Food web paradigms: the biochemical view on trophic interactions. International Review of Hydrobiology 93: 489–505.Google Scholar
  63. Olrik, K., 1998. Ecology of mixotrophic flagellates with special reference to Chrysophyceae in Danish lakes. Hydrobiologia 369(370): 329–338.Google Scholar
  64. Özen, A., Ű. N. Tavşanoğlu, Aİ. Çakıroğlu, E. E. Levi, E. Jeppesen & M. Beklioğlu, 2018. Patterns of microbial food webs in Mediterranean shallow lakes with contrasting nutrient levels and predation pressures. Hydrobiologia 806: 13–27.Google Scholar
  65. Pauli, H. R., 1989. A new method to estimate individual dry weights of rotifers. Hydrobiologia 186–187: 355–361.Google Scholar
  66. Porter, K. G. & Y. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.Google Scholar
  67. Posch, T., B. Eugster, F. Pomati, J. Pernthaler, G. Pitsch & E. M. Eckert, 2015. Network of Interactions Between Ciliates and phytoplankton during spring. Frontiers in Microbiology 6: 1289.PubMedPubMedCentralGoogle Scholar
  68. Putt, M. & D. K. Stoecker, 1989. An experimentally determined carbon: volume ratio for marine oligotrichous ciliates from estuarine and coastal waters. Limnology and Oceanography 34: 1097–1103.Google Scholar
  69. R Development Core Team, 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing.Google Scholar
  70. Rejas, D., K. Muylaert & L. De Meester, 2005. Trophic interactions within the MFW in a tropical floodplain lake (Laguna Bufeos, Bolivia). Revista de Biología Tropical 53.Google Scholar
  71. Reynolds, C. S., 1997. Vegetation processes in the pelagic: a model for ecosystem theory. International Ecology Institute (ECI), Oldendorf/Luhe, Germany.Google Scholar
  72. Rocha, O. & A. Duncan, 1985. The relationship between cell carbon and cell volume in freshwater algal species used in zooplanktonic studies. Journal of Plankton Research 7: 279–294.Google Scholar
  73. Roland, F., L. M. Lobão, L. O. Vidal, E. Jeppesen, R. Paranhos & V. L. M. Huszar, 2010. Relationships between pelagic bacteria and phytoplankton abundances in contrasting tropical freshwaters. Aquatic Microbial Ecology 60: 261–272.Google Scholar
  74. Rosseel, Y., 2014. Structural Equation Modeling with lavaan. 1–128.Google Scholar
  75. Ruttner-Kolisko, A., 1977. Suggestions for biomass calculation of plankton rotifers. Archiv für Hydrobiologie, Beihefte, Ergebnisse der Limnologie 8: 71–76.Google Scholar
  76. Sarmento, H., 2012. New paradigms in tropical limnology: the importance of the microbial food web. Hydrobiologia 686: 1–14.Google Scholar
  77. Sarmento, H., F. Unrein, M. Isumbisho, S. Stenuite, J. M. Gasol & J.-P. Descy, 2008. Abundance and distribution of picoplankton in tropical, oligotrophic Lake Kivu, eastern Africa. Freshwater Biology 53: 756–771.Google Scholar
  78. Sas, H., 1989. Lake Restoration by Reduction of Nutrient Loading Expectation, Experiences, Extrapolation. Academia Verlag Richardz, St. Augustin: 497.Google Scholar
  79. Schindler, D. E., S. R. Carpenter, J. J. Cole, J. F. Kitchell & M. L. Pace, 1997. Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 277: 248–251.Google Scholar
  80. Segovia, B. T., D. G. Pereira, L. M. Bini, B. R. Meira, V. S. Nishida, F. A. Lansac-Tôha & L. F. M. Velho, 2015. The role of microorganisms in a planktonic food web of a floodplain lake. Microbial Ecology 69: 225–233.PubMedGoogle Scholar
  81. Segovia, B. T., C. D. Domingues, B. R. Meira, F. M. Lansac-Toha, P. Fermani, F. Unrein, L. M. Lobao, F. Roland, L. F. Velho & H. Sarmento, 2016. Coupling between heterotrophic nanoflagellates and bacteria in fresh waters: does latitude make a difference? Frontiers in Microbiology 7: 114.PubMedPubMedCentralGoogle Scholar
  82. Segovia, B. T., B. R. Meira, F. M. Lansac-Toha, F. E. Amadeo, F. Unrein, L. F. M. Velho & H. Sarmento, 2018. Growth and cytometric diversity of bacterial assemblages under different top-down control regimes by using a size-fractionation approach. Journal of Plankton Research 40: 129–141.Google Scholar
  83. Silva, L. H. S., V. L. M. Huszar, M. M. Marinho, L. M. Rangel, J. Brasil, C. C. Domingues, C. C. Branco & F. Roland, 2014. Drivers of phytoplankton, bacterioplankton, and zooplankton carbon biomass in tropical hydroelectric reservoirs. Limnologica 48: 1–10.Google Scholar
  84. Šimek, K., M. Macek, J. Pernthaler, V. Straškrabová & R. Psenner, 1996. Can freshwater planktonic ciliates survive on a diet of picoplankton? Journal of Plankton Research 18: 597–613.Google Scholar
  85. Šimek, K., K. Hornák, M. Masín, U. Christaki, J. Nedoma, M. G. Weinbauer & J. R. Dolan, 2003. Comparing the effects of resource enrichment and grazing on a bacterioplankton community of a meso-eutrophic reservoir. Aquatic Ecology 31: 123–135.Google Scholar
  86. Šimek, K., K. Horňák, J. Jezbera, M. Mašín, J. Nedoma, J. M. Gasol & M. Schauer, 2005. Influence of top-down and bottom-up manipulation on the R-BT065 subcluster of β-Proteobacteria, an abundant group in bacterioplankton of a freshwater reservoir. Applied and Environmental Microbiology 71: 2381–2390.PubMedPubMedCentralGoogle Scholar
  87. Sioli, H., 1984. The Amazon and its main affluents: hydrography, morphology of the river types. In Sioli, H. (ed.), The Amazon: limnology and landscape ecology of a mighty tropical river and its basin. Dr. W. Junk Publishers, Dordrecht: 127–166.Google Scholar
  88. Steiger, J. H., 2007. Understanding the limitations of global fit assessment in structural equation modeling. Personality and Individual Differences 42: 893–898.Google Scholar
  89. Stockner, J. G. & K. S. Shortreed, 1991. Phototrophic picoplankton: community composition, abundance and distribution across a gradient of oligotrophic Columbia and Yukon Territory lakes. Internationale Revue der gesamten Hydrobiologie und Hydrographie 76: 581–601.Google Scholar
  90. Uehlinger, V., 1964. Étude statistique des méthodes de dénombrement planctonique. Archives des Sciences 17: 121–223.Google Scholar
  91. Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Internationale Vereinigung für theoretische und angewandte Limnologie: Mitteilungen 9: 1–38.Google Scholar
  92. Vidal, L. O., G. Abril, L. F. Artigas, M. L. Melo, M. C. Bernardes, L. M. Lobão, M. C. Reis, P. Moreira-Turcq, M. Benedetti, V. L. Tornisielo & F. Roland, 2015. Hydrological pulse regulating the bacterial heterotrophic metabolism between Amazonian mainstems and floodplain lakes. Frontiers in Microbiology.  https://doi.org/10.3389/fmicb.2015.01054.CrossRefPubMedPubMedCentralGoogle Scholar
  93. Ward, B. A. & M. J. Follows, 2016. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proceedings of the National Academy of Sciences of the USA 113: 2958–2963.PubMedGoogle Scholar
  94. Wetzel, R. G. & G. E. Likens, 2000. Composition and Biomass of Phytoplankton. In Wetzel, R. G. & G. E. Likens (eds), Limnological Analyses, 3rd ed. Springer, New York: 147–154.Google Scholar
  95. Zubkov, M. V., M. A. Sleigh, G. A. Tarran, P. H. Burkill & R. J. G. Leakey, 1998. Picoplanktonic community structure on an Atlantic transect from 50°N to 50°. Deep-Sea Research I 45: 1339–1355.Google Scholar

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Authors and Affiliations

  1. 1.Laboratory of Environmental BiogeochemistryFederal University of RondôniaPôrto VelhoBrazil
  2. 2.Laboratory of Phycology, Department of Botany, National MuseumFederal University of Rio de JaneiroRio de JaneiroBrazil
  3. 3.Laboratory of Hydrobiology, Department of Marine Biology, Institute of BiologyFederal University of Rio de JaneiroRio de JaneiroBrazil
  4. 4.Laboratory of Aquatic Ecology, Department of Biology, Institute of BiologyFederal University of Juiz de ForaJuiz de ForaBrazil
  5. 5.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  6. 6.Biosciences Institute, Federal University of the Rio de Janeiro StateRio de JaneiroBrazil
  7. 7.Laboratory of Microbial Processes and Biodiversity, Department of HydrobiologyFederal University of São CarlosSão CarlosBrazil

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