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Aquatic Sciences

, 81:49 | Cite as

The El Niño Southern Oscillation (ENSO) is the main source of variation for the gamma diversity of plankton communities in subtropical shallow lakes

  • Alfonso PinedaEmail author
  • Óscar Peláez
  • Juliana Déo Dias
  • Bianca Trevizan Segovia
  • Cláudia Costa Bonecker
  • Luiz Felipe Machado Velho
  • Luzia Cleide Rodrigues
Research Article

Abstract

We determined the variation in the composition of plankton communities (zooplankton, phytoplankton, and ciliates) in subtropical lakes at different temporal scales, in relation to the seasons (dry and rainy seasons), as well as at finer (among months) and broader (ENSO—among El Niño, La Niña, and normal climate events) scales. Using a 16-year time-series dataset, we tested the hypothesis that seasonal variation would explain most of the gamma diversity of these plankton communities. We also investigated the environmental and temporal factors responsible for the variations in composition and species turnover. The scale related to dry and rainy seasons explained a considerable percentage of the gamma diversity and variation partitioning, showed that compositional changes occurred mainly over broader temporal scales. Environmental factors varying among seasons and ENSO events explained changes in composition, although some communities did not respond to the environment. Our results suggest that niche and stochastic processes operating at temporal scales correlated with ENSO climate events contributed to changes in species composition. Hence, climate anomalies might be important to maintain diversity in areas with reduced or loss of the natural variations in environmental conditions. Our results also suggest that, although communities show similar patterns of variation in composition, they might respond in a different degree to environmental and temporal factors. Thus, while niche-associated (environment) and stochastic (time) processes drove the phytoplankton, stochastic processes were more important for zooplankton, whereas neither were important for ciliates.

Keywords

Plankton diversity El Niño La Niña Floodplain Shallow lakes Flood pulse 

Notes

Acknowledgments

We thank Dr. Luis M. Bini, Dr. Liliana Rodrigues, Dr. Roger Paulo Mormul, and Dr. Nadson R. Simões for valuable comments on the first version of this manuscript. We also acknowledge three anonymous referees for providing valuable suggestions that significantly improved the quality of the manuscript. We thank Nupélia and PELD (site 6)/CNPq for logistic and financial support. CAPES provided a scholarship to AP and CNPq provided Grants to OP. All authors have contributed substantially to this work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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References

  1. Abrahams C (2008) Climate change and lakeshore conservation: a model and review of management techniques. Hydrobiologia 613:33–43.  https://doi.org/10.1007/s10750-008-9470-5 CrossRefGoogle Scholar
  2. Agostinho AA, Thomaz SM, Gomes LC (2004) Threats for biodiversity in the floodplain of the Upper Paraná River: effects of hydrological regulation by dams. Ecohydrol Hydrobiol 4:255–256Google Scholar
  3. Agostinho AA, Thomaz SM, Gomes LC (2005) Conservation of the biodiversity of Brazil’s inland waters. Conserv Biol 19:646–652.  https://doi.org/10.1111/j.1523-1739.2005.00701.x CrossRefGoogle Scholar
  4. Agostinho AA, Gomes LC, Pelicice FM (2007) Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. EDUEM, MaringáGoogle Scholar
  5. Agostinho AA, Bonecker CC, Gomes LC (2009) Effects of water quantity on connectivity: the case of the upper Paraná River floodplain. Ecohydrol Hydrobiol 9:99–113.  https://doi.org/10.2478/v10104-009-0040-x CrossRefGoogle Scholar
  6. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525CrossRefGoogle Scholar
  7. Andersson MGI, Berga M, Lindström ES, Langenheder S (2014) The spatial structure of bacterial communities is influenced by historical envirionmental conditions. Ecology 95:1134–1140CrossRefGoogle Scholar
  8. Angeler DG, Johnson RK (2012) Patterns of temporal community turnover are spatially synchronous across boreal lakes. Freshw Biol 57:1782–1793.  https://doi.org/10.1111/j.1365-2427.2012.02838.x CrossRefGoogle Scholar
  9. Angeler DG, Drakare S, Johnson RK (2011) Revealing the organization of complex adaptive systems through multivariate time series modeling. Ecol Soc.  https://doi.org/10.5751/es-04175-160305 CrossRefGoogle Scholar
  10. Anneville O, Souissi S, Ibanez F et al (2002) Temporal mapping of phytoplankton assemblages in Lake Geneva: annual and interannual changes in their patterns of succession. Limnol Oceanogr 47:1355–1366.  https://doi.org/10.4319/lo.2002.47.5.1355 CrossRefGoogle Scholar
  11. Attayde JL, Bozelli RL (1998) Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis. Can J Fish Aquat Sci 55:1789–1797.  https://doi.org/10.1139/cjfas-55-8-1789 CrossRefGoogle Scholar
  12. Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143CrossRefGoogle Scholar
  13. Beck J, Holloway JD, Khen CV, Kitching IJ (2012) Diversity partitioning confirms the importance of beta components in tropical rainforest Lepidoptera. Am Nat 180:E64–E74.  https://doi.org/10.1086/666982 CrossRefPubMedGoogle Scholar
  14. Beisner BE, Peres-Neto PR, Lindström ES et al (2006) The role of environmental and spatial processes in structuring lake communities from bacteria to fish. Ecology 87:2985–2991.  https://doi.org/10.1890/0012-9658(2006)87%5b2985:TROEAS%5d2.0.CO;2 CrossRefPubMedGoogle Scholar
  15. Blanchet FG (2009) AEM: tools to construct asymmetric eigenvector maps (AEM) spatial variables. R Package Version 0.5-1/r118. http://R-Forge.R-project.org/projects/sedar/i
  16. Blanchet FG, Legendre P, Borcard D (2008a) Modelling directional spatial processes in ecological data. Ecol Modell 215:325–336.  https://doi.org/10.1016/j.ecolmodel.2008.04.001 CrossRefGoogle Scholar
  17. Blanchet GF, Legendre P, Borcard D (2008b) Forward selection of explanatory variables. Ecology 89:2623–2632.  https://doi.org/10.1890/07-0986.1 CrossRefPubMedGoogle Scholar
  18. Borcard D, Gillet F, Legendre P (2011) Numerical Ecology with R. Springer, New YorkCrossRefGoogle Scholar
  19. Bortolini JC, Train S, Rodrigues LC (2016) Extreme hydrological periods: effects on phytoplankton variability and persistence in a subtropical floodplain. Hydrobiologia 763:223–236.  https://doi.org/10.1007/s10750-015-2378-y CrossRefGoogle Scholar
  20. Bortolini JC, Pineda A, Rodrigues LC et al (2017) Environmental and spatial processes influencing phytoplankton biomass along a reservoirs-river-floodplain lakes gradient: a metacommunity approach. Freshw Biol 62:1756–1767.  https://doi.org/10.1111/fwb.12986 CrossRefGoogle Scholar
  21. Bottrell HH, Duncan A, Gliwicz ZM et al (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456Google Scholar
  22. Bovo-Scomparin VM, Train S (2008) Long-term variability of the phytoplankton community in an isolated floodplain lake of the Ivinhema river state park, Brazil. Hydrobiologia 610:331–344.  https://doi.org/10.1007/s10750-008-9448-3 CrossRefGoogle Scholar
  23. Bozelli RL, Thomaz SM, Padial AA et al (2015) Floods decrease zooplankton beta diversity and environmental heterogeneity in an Amazonian floodplain system. Hydrobiologia 753:233–241.  https://doi.org/10.1007/s10750-015-2209-1 CrossRefGoogle Scholar
  24. Braghin LSM, Simões NR, Bonecker CC (2016) Hierarchical effects of local factors on zooplankton species diversity. Inland Waters 6:645–654.  https://doi.org/10.5268/IW-6.4.919 CrossRefGoogle Scholar
  25. Chao A, Chiu CH, Hsieh TC, Inouye BD (2012) Proposing a resolution to debates on diversity partitioning. Ecology 93:2037–2051.  https://doi.org/10.1890/11-1817.1 CrossRefPubMedGoogle Scholar
  26. Chaparro G, Horváth Z, O’Farrell I et al (2018) Plankton metacommunities in floodplain wetlands under contrasting hydrological conditions. Freshw Biol 63:380–391CrossRefGoogle Scholar
  27. Chase JM, Kraft NJB, Smith KG et al (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:24.  https://doi.org/10.1890/es10-00117.1 CrossRefGoogle Scholar
  28. Cheng H, Sinha A, Cruz FW et al (2013) Climate change patterns in Amazonia and biodiversity. Nat Commun 4:1411.  https://doi.org/10.1038/ncomms2415 CrossRefPubMedGoogle Scholar
  29. Chesson PL, Warner RR (1981) Environmental variable promotes coexistence in lottery competitive systems. Am Nat 117:923–943CrossRefGoogle Scholar
  30. Cole AG (1994) Textbook of Limnology, 4th edn. Waveland Press, Inc., Prospect HeightsGoogle Scholar
  31. Coombes KR, Wang M (2018) PCDimension: finding the number of significant principal components. R package version 1.1.9Google Scholar
  32. Crist TO, Veech JA (2006) Additive partitioning of rarefaction curves and species-area relationships: unifying α-, β- and γ-diversity with sample size and habitat area. Ecol Lett 9:923–932.  https://doi.org/10.1111/j.1461-0248.2006.00941.x CrossRefPubMedGoogle Scholar
  33. Crist TO, Veech JA, Gering JC, Summerville KS (2003) Partitioning species diversity across landscapes and regions: a hierarchical analysis of alpha, beta, and gamma diversity. Am Nat 162:734–743.  https://doi.org/10.1086/378901 CrossRefPubMedGoogle Scholar
  34. De Bie T, De Meester L, Brendonck L et al (2012) Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol Lett 15:740–747.  https://doi.org/10.1111/j.1461-0248.2012.01794.x CrossRefPubMedGoogle Scholar
  35. De Boeck HJ, Bloor JMG, Kreyling J et al (2018) Patterns and drivers of biodiversity-stability relationships under climate extremes. J Ecol 106:890–902.  https://doi.org/10.1111/1365-2745.12897 CrossRefGoogle Scholar
  36. Deflandre G (1929) Le genre centropyxis Stein. Arch für Protistenkd 67:322–375Google Scholar
  37. Dittrich J, Dias JD, Bonecker CC et al (2016) Importance of temporal variability at different spatial scales for diversity of floodplain aquatic communities. Freshw Biol 61:316–327.  https://doi.org/10.1111/fwb.12705 CrossRefGoogle Scholar
  38. Dolan JR (2005) An introduction to the biogeography of aquatic microbes. Aquat Microb Ecol 41:39–48.  https://doi.org/10.3354/ame041039 CrossRefGoogle Scholar
  39. Dornelas M (2010) Disturbance and change in biodiversity. Philos Trans R Soc Lond B Biol Sci 365:3719–3727CrossRefGoogle Scholar
  40. Elmoor-Loureiro MAL (1997) Manual de identificação de cladóceros límnicos do Brasi. Editora Universa, BrasíliaGoogle Scholar
  41. Evans S, Martiny JBH, Allison SD (2017) Effects of dispersal and selection on stochastic assembly in microbial communities. ISME J 11:176–185.  https://doi.org/10.1038/ismej.2016.96 CrossRefPubMedGoogle Scholar
  42. Franklin JF (1989) Importance and justification of long-term studies in ecology. In: Likens GE (ed) long-term studies in ecology. Springer, New York, pp 3–19CrossRefGoogle Scholar
  43. Fukami T, Bezemer TM, Mortimer SR, Van Der Putten WH (2005) Species divergence and trait convergence in experimental plant community assembly. Ecol Lett 8:1283–1290.  https://doi.org/10.1111/j.1461-0248.2005.00829.x CrossRefGoogle Scholar
  44. Gauthier-Lièvre L, Thomas R (1958) Le genre Difflugia, Pentagonia, Maghrebia et Hoogenraadia (Rhizopodes Testacès) en Afrique. Arch für Protistenkd 103:1–370Google Scholar
  45. Gering JC, Crist TO, Veech JA (2003) Additive partitioning of species diversity across multiple spatial scales: implications for regional conservation of biodiversity. Conserv Biol 17(2):488–499CrossRefGoogle Scholar
  46. Gimmler A, Korn R, de Vargas C, Audic S, Stoeck T (2016) The Tara Oceans voyage reveals global diversity and distribution patterns of marine planktonic ciliates. Sci Rep  https://doi.org/10.1038/srep33555
  47. Gotelli NJ, Colwell RK (2001) Estimating species richness. In: Magurran AE (ed) Frontiers in measuring biodiversity. Oxford University Press, New YorkGoogle Scholar
  48. Gotelli NJ, Shimadzu H, Dornelas M et al (2017) Community-level regulation of temporal trends in biodiversity. Sci Adv 3:e1700315CrossRefGoogle Scholar
  49. Grinnell J (1917) The niche-relationships of the California thrasher. Auk 34:427–433.  https://doi.org/10.2307/4072271 CrossRefGoogle Scholar
  50. Hallett LM, Hsu JS, Cleland EE et al (2014) Biotic mechanisms of community stability shift along a precipitation gradient. Ecology 95:1693–1700CrossRefGoogle Scholar
  51. Hastings A, Abbott KC, Cuddington K et al (2018) Transient phenomena in ecology. Science 361:eaat6412.  https://doi.org/10.1126/science.aat6412 CrossRefPubMedGoogle Scholar
  52. Heino J (2010) Are indicator groups and cross-taxon congruence useful for predicting biodiversity in aquatic ecosystems? Ecol Indic 10:112–117.  https://doi.org/10.1016/j.ecolind.2009.04.013 CrossRefGoogle Scholar
  53. Heino J, Melo AS, Bini LM (2015a) Reconceptualising the beta diversity-environmental heterogeneity relationship in running water systems. Freshw Biol 60:223–235.  https://doi.org/10.1111/fwb.12502 CrossRefGoogle Scholar
  54. Heino J, Melo AS, Siqueira T et al (2015b) Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshw Biol 60:845–869.  https://doi.org/10.1111/fwb.12533 CrossRefGoogle Scholar
  55. Hessen DO, Faafeng BA, Smith VH et al (2006) Extrinsic and intrinsic controls of zooplankton diversity in lakes. Ecology 87:433–443.  https://doi.org/10.1890/05-0352 CrossRefPubMedGoogle Scholar
  56. Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. In: Dodge DP (eds) In: Proceedings of the international large river symposium. Canadian Special Publication Fisheries and Aquatic Sciences, Otawa, 106:110–127Google Scholar
  57. Kent AD, Yannarell AC, Rusak JA et al (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47.  https://doi.org/10.1038/ismej.2007.6 CrossRefPubMedGoogle Scholar
  58. Koste W (1978) Rotatoria die Rädertiere Mitteleuropas begründet von Max Voight. Monogononta. Gebrüder Borntraeger, BerlinGoogle Scholar
  59. Küppers GC, Claps MC (2012) Spatiotemporal variations in abundance and biomass of planktonic ciliates related to environmental variables in a temporal pond, Argentina. Zool Stud 51:298–313Google Scholar
  60. Lande R (1996) Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76:5–13CrossRefGoogle Scholar
  61. Lansac-Tôha FM, Meira BR, Segovia BT et al (2016) Hydrological connectivity determining metacommunity structure of planktonic heterotrophic flagellates. Hydrobiologia 781:81–94.  https://doi.org/10.1007/s10750-016-2824-5 CrossRefGoogle Scholar
  62. Legendre P (2014) Interpreting the replacement and richness difference components of beta diversity. Global Ecol Biogeogr 23:1324–1334.  https://doi.org/10.1111/geb.12207 CrossRefGoogle Scholar
  63. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129(2):271–280CrossRefGoogle Scholar
  64. Legendre P, Gauthier O (2014) Statistical methods for temporal and space-time analysis of community composition data. Proc R Soc B Biol Sci 281:20132728.  https://doi.org/10.1098/rspb.2013.2728 CrossRefGoogle Scholar
  65. Leibold MA, Chase JM (2018a) Metacommunity patterns in space. In: Leibold MA, Chase JM (eds) Metacommunity ecology2. Princeton University Press, Princeton, pp 90–130CrossRefGoogle Scholar
  66. Leibold MA, Chase JM (2018b) Interactions between time and space in metacommunities. In: Leibold MA, Chase JM (eds) Metacommunity ecology. Princeton University Press, Princeton, pp 131–150CrossRefGoogle Scholar
  67. Lund JWG, Kipling C, Le Cren EDE (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:980–985.  https://doi.org/10.1007/BF00007865 CrossRefGoogle Scholar
  68. MacArthur R (1965) Patterns of species diversity. Biol Rev Camb Philos Soc 40:510–533CrossRefGoogle Scholar
  69. Madoni P (1984) Estimation of the size of freshwater ciliate populations by a sub-sampling technique. Hydrobiologia 111:201–206.  https://doi.org/10.1007/BF00007200 CrossRefGoogle Scholar
  70. Magurran AE, Deacon AE, Moyes F et al (2018) Divergent biodiversity change within ecosystems. Proc Natl Acad Sci.  https://doi.org/10.1073/pnas.1712594115 CrossRefPubMedGoogle Scholar
  71. Matsumura-Tundisi T (1986) Latitudinal distribution of Calanoida copepods in freshwater aquatic systems of Brazil. Braz J Biol 46:527–553Google Scholar
  72. Medley KA, Havel JE (2007) Hydrology and local environmental factors influencing zooplankton communities in floodplain ponds. Wetlands 27:864–872CrossRefGoogle Scholar
  73. Neiff JJ (1990) Ideas para la interpretación ecológica del Paraná. Interciencia 15:424–441Google Scholar
  74. Oksanen MJ, Blanchet FG, Kindt R et al (2012) vegan: Community Ecology Package. R package version 2.5-4Google Scholar
  75. Padial AA, Ceschin F, Declerck SAJ et al (2014) Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS ONE 9:e111227.  https://doi.org/10.1371/journal.pone.0111227 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.  https://doi.org/10.1093/bioinformatics/btg412 CrossRefPubMedGoogle Scholar
  77. Pecl GT, Araújo MB, Bell JD et al (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355:eaai9214.  https://doi.org/10.1126/science.aai9214 CrossRefGoogle Scholar
  78. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625CrossRefGoogle Scholar
  79. Purves AW, Pacala SW (2005) Ecological drift in niche-structured communities: neutral pattern does not imply neutral processes. In: Burslem D, Pinard M, Hartley S (eds) Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge University Press, New York, pp 107–140CrossRefGoogle Scholar
  80. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org
  81. Reid LW (1985) Chave de identificação e lista de referências bibliográficas para as espécies continentais sulamericanas de vida livre da ordem Cyclopoida (Crustacea, Copepoda). Bol Zool USP 9:17–143CrossRefGoogle Scholar
  82. Rodríguez-Ramos T, Dornelas M, Marañón E, Cermeño P (2014) Conventional sampling methods severely underestimate phytoplankton species richness. J Plankton Res 36(2):334–343CrossRefGoogle Scholar
  83. Segers H (1995) The Lecanidae (Monogononta). Guides to the identification of the Microinvertebrates of the Continental waters of the world 6. PB Academic Publishing, KolkataGoogle Scholar
  84. Segovia BT, Dias JD, Cabral AF et al (2017) Common and rare taxa of planktonic ciliates: influence of flood events and biogeographic patterns in Neotropical floodplains. Microb Ecol.  https://doi.org/10.1007/s00248-017-0974-2 CrossRefPubMedGoogle Scholar
  85. Simões NR, Lansac-Tôha FA, Velho LFM, Bonecker CC (2012) Intra and inter-annual structure of zooplankton communities in floodplain lakes: a long-term ecological research study. Rev Biol Trop 60:1819–1836CrossRefGoogle Scholar
  86. Simões NR, Dias JD, Leal CM et al (2013) Floods control the influence of environmental gradients on the diversity of zooplankton communities in a neotropical floodplain. Aquat Sci 75:607–617.  https://doi.org/10.1007/s00027-013-0304-9 CrossRefGoogle Scholar
  87. Smith TW, Lundholm JT (2010) Variation partitioning as a tool to distinguish between niche and neutral processes. Ecography (Cop) 33:648–655.  https://doi.org/10.1111/j.1600-0587.2009.06105.x CrossRefGoogle Scholar
  88. Solari LC, Gabellone NA, Claps MC et al (2014) Phytoplankton chlorophyte structure as related to ENSO events in a saline lowland river (Salado River, Buenos Aires, Argentina). Ecol Evol 4:918–932.  https://doi.org/10.1002/ece3.983 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Souza Filho E (2009) Evaluation of the Upper Paraná River discharge controlled by reservoirs. Braz J Biol 69:707–716CrossRefGoogle Scholar
  90. Souza Filho EE, Stevaux JC (1997) Geologia e geomorfologia do complexo rio Baia, Corutuba, Ivinhema. In: Vazzoler AE, Agostinho AA, Hahn NS (eds) A Planície de inundação do alto rio Paraná: aspectos limnológicos e sócio-econômicos. EDUEM, Maringá, pp 3–43Google Scholar
  91. Souza Filho EE, Rocha PC, Comunello E, Stevaux JC (2004) Effects of the Porto Primavera Dam on physical environment of the downstream floodplain. In: Thomaz SM, Agostinho A, Hanh NS (eds) The upper Paraná river and its floodplain: physical aspects, ecology and conservation. Backhuys Pubblishers, Leiden, pp 55–74Google Scholar
  92. Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17:866–880.  https://doi.org/10.1111/ele.12277 CrossRefPubMedGoogle Scholar
  93. Steiner CF (2014) Stochastic sequential dispersal and nutrient enrichment drive beta diversity in space and time. Ecology 95:2603–2612CrossRefGoogle Scholar
  94. Su J, Tian T, Krasemann H et al (2015) Response patterns of phytoplankton growth to variations in resuspension in the German Bight revealed by daily MERIS data in 2003 and 2004. Oceanologia 57:328–341.  https://doi.org/10.1016/j.oceano.2015.06.001 CrossRefGoogle Scholar
  95. Sun J, Liu D (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25:1331–1346.  https://doi.org/10.1093/plankt/fbg096 CrossRefGoogle Scholar
  96. Ter Braak C (1988) CANOCO—a Fortran program for canonical community ordination by [partial] [detrended][canonical] correspondence analysis, principal component analysis and redundancy analysis. (version 2.1), Report LWA-88-02. Agricultural Mathematics Group, Wageningen, NetherlandsGoogle Scholar
  97. They NH, Ferreira LMH, Marins LF, Abreu PC (2015) Bacterial community composition and physiological shifts associated with the El Niño Southern Oscillation (ENSO) in the Patos Lagoon Estuary. Microb Ecol 69:525–534.  https://doi.org/10.1007/s00248-014-0511-5 CrossRefPubMedGoogle Scholar
  98. Thomas MK, Fontana S, Reyes M et al (2018) The predictability of a lake phytoplankton community, over time-scales of hours to years. Ecol Lett 21:619–628CrossRefGoogle Scholar
  99. Tonkin JD, Altermatt F, Finn DS et al (2018) The role of dispersal in river network metacommunities: patterns, processes, and pathways. Freshw Biol 63:141–163.  https://doi.org/10.1111/fwb.13037 CrossRefGoogle Scholar
  100. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen der Int Vereinigung für Theor und Angew Limnol 9:1–38Google Scholar
  101. Vasseur DA, Fox JW, Gonzalez A et al (2014) Synchronous dynamics of zooplankton competitors prevail in temperate lake ecosystems. Proc R Soc B Biol Sci 281:20140633.  https://doi.org/10.1098/rspb.2014.0633 CrossRefGoogle Scholar
  102. Xu H, Yong J, Xu G (2015) Sampling frequency of ciliated protozoan microfauna for seasonal distribution research in marine ecosystems. Mar Pollut Bull 101:653–659.  https://doi.org/10.1016/j.marpolbul.2015.10.034 CrossRefPubMedGoogle Scholar
  103. Zhang M, Chen F, Shi X et al (2018) Association between temporal and spatial beta diversity in phytoplankton. Ecography 41:1345–1356CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alfonso Pineda
    • 1
    Email author
  • Óscar Peláez
    • 1
  • Juliana Déo Dias
    • 2
  • Bianca Trevizan Segovia
    • 3
  • Cláudia Costa Bonecker
    • 1
    • 4
  • Luiz Felipe Machado Velho
    • 1
    • 4
    • 5
  • Luzia Cleide Rodrigues
    • 1
    • 4
  1. 1.Programa de Pós-graduação em Ecologia de Ambientes Aquáticos ContinentaisUniversidade Estadual de Maringá, Avenida ColomboMaringá, ParanáBrazil
  2. 2.Departamento de Oceanografia e Limnologia. Via Costeira Senador Dinarte Medeiros MarizUniversidade Federal do Rio Grande do NorteNatalBrazil
  3. 3.Department of BotanyUniversity of British ColumbiaVancouverCanada
  4. 4.Núcleo de Pesquisas em Limnologia, Ictiologia e AquiculturaUniversidade Estadual de MaringáMaringáBrazil
  5. 5.Programa de Pós-graduação em Tecnologias Limpas (PPGTL)UnicesumarMaringáBrazil

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