Abstract
In floodplain lakes, precipitation events shape the environmental heterogeneity and the occurrence of species and functional traits. However, the importance of each biotic and abiotic factor on structuring communities might depend on the local environmental conditions and the identity of such communities. We investigated through Permutational analyses of variance and functional β-diversity components, the effects of neutral and extreme events of precipitation on environmental heterogeneity and distribution of zooplankton functional traits in floodplain lakes. We also examined through distance-based redundancy analysis and fourth-corner analysis, how different variables (physical–chemical, food availability, predation, and temporal dynamics) structure the distribution of zooplankton functional traits and which traits were related to these variables. We used data from six lakes of the Upper Paraná River floodplain over 19 years. Environmental heterogeneity and β-diversity were higher during El Niño and lower during La Niña (extreme rainy and extremely dry season, respectively). Physical–chemical were the variables that most explained zooplankton β-diversity during all seasons and predation during both extreme seasons (La Niña and El Niño). We observed a set of multiple biotic and abiotic factors causing complex effects on zooplankton functional diversity. The homogenization of traits—observed during extreme dry seasons—can lead to losses in ecosystem functions and services if these events continue to be more frequent and intense. We reaffirm the importance of natural flood caused by the rainy seasons to maintain high biotic and abiotic heterogeneity and ecosystem processes.
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References
Agostinho AA, Zalewski M (1996) A planície de inundação do alto rio Paraná: importância e preservação. Eduem, Maringá
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 4:255–268
Antiqueira PAP, Petchey OL, dos Santos VP et al (2018) Environmental change and predator diversity drive alpha and beta diversity in freshwater macro and microorganisms. Glob Change Biol 24:3715–3728. https://doi.org/10.1111/gcb.14314
Auer B, Elzer U, Arndt H (2004) Comparison of pelagic food webs in lakes along a trophic gradient and with seasonal aspects: Influence of resource and predation. J Plankton Res 26:697–709. https://doi.org/10.1093/plankt/fbh058
Barnett AJ, Finlay K, Beisner BE (2007) Functional diversity of crustacean zooplankton communities: towards a trait-based classification. Freshw Biol 52:796–813. https://doi.org/10.1111/j.1365-2427.2007.01733.x
Bertoncin APS, Pinha GD, Baumgartner MT, Mormul RP (2019) Extreme drought events can promote homogenization of benthic macroinvertebrate assemblages in a floodplain pond in Brazil. Hydrobiologia 826:379–393. https://doi.org/10.1007/s10750-018-3756-z
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632
Bolar K (2019) STAT: interactive document for working with basic statistical analysis. R package version 0.1.0. https://CRAN.R-project.org/package=STAT
Bomfim FF, Braghin LSM, Bonecker CC, Lansac-Tôha FA (2018) High food availability linked to dominance of small zooplankton in a subtropical floodplain. Int Rev Hydrobiol 103:26–34. https://doi.org/10.1002/iroh.201701923
Bougeard S, Dray S (2018) Supervised multiblock analysis in R with the ade4 package. J Stat Softw 86:1–17. https://doi.org/10.18637/jss.v086.i01
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
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
Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1890/03-9000
Cai W, Borlace S, Lengaigne M et al (2014) Increasing frequency of El Niño events due to greenhouse warming. Nat Clim Change 4:111–116
Cai W, Santoso A, Wang G et al (2015) ENSO and greenhouse warming. Nat Clim Change 5:849–859
Cardoso P, Mammola S, Rigal F, Carvalho JC (2020) BAT: biodiversity assessment tools. R package version 2.5.0. https://CRAN.R-project.org/package=BAT
Carvalho JC, Cardoso P, Gomes P (2012) Determining the relative roles of species replacement and species richness differences in generating beta-diversity patterns. Glob Ecol Biogeogr 21:760–771. https://doi.org/10.1111/j.1466-8238.2011.00694.x
Cavalcantti IFA, Carril AF, Penalba OC et al (2015) Precipitation extremes over La Plata Basin—review and new results from observations and climate simulations. J Hydrol 523:211–230
Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci USA 104:17430–17434. https://doi.org/10.1073/pnas.0704350104
Chase JM, Abrams PA, Grover JP et al (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315. https://doi.org/10.1046/j.1461-0248.2002.00315.x
Colina M, Calliari D, Carballo C, Kruk C (2016) A trait-based approach to summarize zooplankton–phytoplankton interactions in freshwaters. Hydrobiologia 767:221–233. https://doi.org/10.1007/s10750-015-2503-y
Collins MR, Knutti J, Arblaster JL (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner G-K et al (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York
da Graça WJ, Pavanelli CS (2007) Peixes da planície de inundação do alto rio Paraná e áreas adjacentes, 1st edn. EDUEM, Maringá
Sodré, EO, Bozelli ERL (2019) How planktonic microcrustaceans respond to environment and affect ecosystem: a functional trait perspective. Int Aquat Res 11:207–223. https://doi.org/10.1007/s40071-019-0233-x
de Braghin LSM, de Almeida BA, Amaral DC et al (2018) Effects of dams decrease zooplankton functional β-diversity in river-associated lakes. Freshw Biol 63:721–730. https://doi.org/10.1111/fwb.13117
Dias JD, Simoes NR, Meerhoff M et al (2016) Hydrological dynamics drives zooplankton metacommunity structure in a Neotropical floodplain. Hydrobiologia. 781:109–125 https://doi.org/10.1007/s10750-016-2827-2
Dray S, Legendre P (2008) Testing the species traits-environment relationships: the fourth-corner problem revisited. Ecology 89:3400–3412
Dray S, Bauman D, Blanchet G, et al (2020) Adespatial: multivariate multiscale spatial analysis. R package version 0.3-13. https://CRAN.R-project.org/package=adespatial
Fernandes R, Agostinho A, Ferreira E et al (2009) Effects of the hydrological regime on the ichthyofauna of riverine environments of the Upper Paraná River floodplain. Braz J Biol 69:669–680. https://doi.org/10.1590/s1519-69842009000300021
Fernandes IM, Henriques-Silva R, Penha J et al (2014) Spatiotemporal dynamics in a seasonal metacommunity structure is predictable: the case of floodplain-fish communities. Ecography (Cop) 37:464–475
Gianuca AT, Declerck SAJ, Lemmens P, De Meester L (2017) Effects of dispersal and environmental heterogeneity on the replacement and nestedness components of ?-diversity. Ecology 98:525–533. https://doi.org/10.1002/ecy.1666
Gurevitch JJ, Morrison A, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155:435–453
Havens KE (1998) Size structure and energetics in a plankton food web. Oikos 81:346–358
He H, Jin H, Jeppesen E et al (2018) Fish-mediated plankton responses to increased temperature in subtropical aquatic mesocosm ecosystems: Implications for lake management. Water Res 144:304–311. https://doi.org/10.1016/j.watres.2018.07.055
Hébert M-PP, Beisner BE, Maranger R (2017) Linking zooplankton communities to ecosystem functioning: toward an effect-Trait framework. J Plankton Res 39:3–12. https://doi.org/10.1093/plankt/fbw068
Heino J, Melo AS, Siqueira T et al (2015) 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
Heino J, Alahuhta J, Fattorini S, Schmera D (2019) Predicting beta diversity of terrestrial and aquatic beetles using ecogeographical variables: insights from the replacement and richness difference components. J Biogeogr 46:304–315. https://doi.org/10.1111/jbi.13485
Junk W, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain-systems. Can J Fish Aquat Sci 106:110–127. https://doi.org/10.1371/journal.pone.0028909
Kalinowska K, Ejsmont-Karabin J, Rzepecki M et al (2015) Impacts of large-bodied crustaceans on the microbial loop. Hydrobiologia 744:115–125. https://doi.org/10.1007/s10750-014-2066-3
Kane RP (2002) Precipitation anomalies in southern South America associated with a finer classification of El Niño and La Niña events. Int J Climatol 22:357–373
Kruk C, Huszar VLM, Peeters ETHM et al (2010) A morphological classification capturing functional variation in phytoplankton. Freshw Biol 55:614–627. https://doi.org/10.1111/j.1365-2427.2009.02298.x
Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12. https://CRAN.R-project.org/package=FD
Lansac-Tôha F, Bonecker C, Velho L et al (2009) Biodiversity of zooplankton communities in the Upper Paraná River floodplain: interannual variation from long-term studies. Braz J Biol 69:539–549. https://doi.org/10.1590/S1519-69842009000300009
Lansac-Tôha FM, Heino J, Quirino BA et al (2019) Differently dispersing organism groups show contrasting beta diversity patterns in a dammed subtropical river basin. Sci Total Environ 691:1271–1281. https://doi.org/10.1016/j.scitotenv.2019.07.236
Lansac-Tôha FM, Quirino BA, Souza YR et al (2021) The commonality of core biological groups across freshwater food webs. Limnol Oceanogr Early View. https://doi.org/10.1002/lno.11697
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
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
Legendre P, Borcard D, Peres-Neto PR (2005) Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol Monogr 75:435–450
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
Magrin GO, Marengo JA, Boulanger JP et al (2014) Central and South America. In: Barros VR, Field CB, Dokken DJ et al (eds) Climate change 2014: impacts, adaptation, and vulnerability. Part B: regional aspects. Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York, pp 1499–1566
Marengo JA (2006) Mudanças climáticas globais e seus efeitos sobre a biodiversidade: caracterização do clima atual e definição das alterações climáticas para o território brasileiro ao longo do século XXI. MMA, Brasilia
Marengo JA, Liebmann B, Grimm AM et al (2012) Recent developments on the South American monsoon system. Int J Climatol 32:1–21
Mormul RP, Thomaz SM, Agostinho AA et al (2012) Migratory benthic fishes may induce regime shifts in a tropical floodplain pond. Freshw Biol 57:1592–1602
Oksanen J, Blanchet FG, Friendly M, et al (2019) vegan: community ecology package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
ONI GGWS (2019) El Niño and La Niña Years and Intensities—Based on Oceanic Niño Index (ONI). https://ggweather.com/enso/oni.htm. Accessed 25 Feb 2020
Paradis E, Schliep K (2018) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528
Pauleto GM, de Oliveira FR, Segovia BT et al (2017) Intra-annual variation in planktonic ciliate species composition (Protista: Ciliophora) in different strata in a shallow floodplain lake. Acta Limnol Bras 29:e107. https://doi.org/10.1590/s2179-975x5817
Peláez O, Pavanelli CS (2019) Environmental heterogeneity and dispersal limitation explain different aspects of β-diversity in Neotropical fish assemblages. Freshw Biol 64:497–505. https://doi.org/10.1111/fwb.13237
Pelicice F, Agostinho AA, Thomaz SM (2005) Fish assemblages associated with Egeria in a tropical reservoir: investigating the effects of plant biomass and diel period. Acta Oecologica 27:9–16
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data metrices: estimation and comparison of fractions. Ecology 87:2614–2625. https://doi.org/10.2307/20069271
Pineda A, Peláez Ó, Dias JD et al (2019) The El Niño Southern Oscillation (ENSO) is the main source of variation for the gamma diversity of plankton communities in subtropical shallow lakes. Aquat Sci 81:1–15. https://doi.org/10.1007/s00027-019-0646-z
Podani J, Schmera D (2011) A new conceptual and methodological framework for exploring and explaining pattern in presence—absence data. Oikos 120:1625–1638. https://doi.org/10.1111/j.1600-0706.2011.19451.x
R Core Team (2020) R: a language and environment for statistical computing. https://www.r-project.org
Reynalte-Tataje DA, Agostinho AA, Bialetzki A (2013) Temporal and spatial distributions of the fish larval assemblages of the Ivinheima River sub-basin (Brazil). Environ Biol Fishes 96:811–822. https://doi.org/10.1007/s10641-012-0073-7
Ripley B, Venables B, Bates DM, et al (2019) MASS: support functions and datasets for venables and Ripley’s MASS. R package version 7.3-53.1. https://CRAN.R-project.org/package=MASS
Roberto MC, Santana N, Thomaz SM (2009) Limnology in the Upper Paraná River floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Braz J Biol 69:717–725. https://doi.org/10.1590/S1519-69842009000300025
Rodriguez MA, Lewis-Jr WM (1997) Structure of fish assemblages along environmental gradients in floodplain lakes of the Orinoco River. Ecol Monogr 67:109–128
Santangelo JM, Soares BN, Paes T et al (2018) Effects of vertebrate and invertebrate predators on the life history of Daphnia similis and Moina macrocopa (Crustacea: Cladocera). Ann Limnol Int J Limnol 54:25. https://doi.org/10.1051/limn/2018015
Scheffer M, Hosper SH, Meijer ML et al (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279
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 74:522–533. https://doi.org/10.1007/s00248-017-0974-2
Serra T, Vidal J, Casamitjana X et al (2007) The role of surface vertical mixing in phytoplankton distribution in a stratified reservoir. Limnol Oceanogr 52:620–634. https://doi.org/10.4319/lo.2007.52.2.0620
Simoes NR, Lansac-Toha FA, Velho LFM, Bonecker CC (2012) Infra and inter-annual structure of zooplankton communities in floodplain lakes: a long-term ecological research study. Rev Biol Trop 60:1819–1836
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
Sparks RE, Spink A (1998) Disturbance, succession and ecosystem processes in rivers and estuaries: effects of extreme hydrologic events. Regul Rivers Res Manag 14:155–159
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
Sun J, Liu D (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25:1331–1346
ter Braak C, Cormont A, Dray S (2012) Improved testing of species traits-environment relationships in the fourth corner problem. Ecology 93:1525–1526
Thomaz SM, Bini LM, Bozelli RL (2007) Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579:1–13. https://doi.org/10.1007/s10750-006-0285-y
Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phyto- plankton-Methodik. Mitteilungen der Int Vereinigung für Theor und Angew Limnol 9:1–38
Ward PJ, Jongman B, Kummu M et al (2014) Strong influence of El Niño Southern Oscillation on flood risk around the world. Proc Natl Acad Sci USA 111:15659–15664. https://doi.org/10.1073/pnas.1409822111
Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363. https://doi.org/10.1146/annurev.ecolsys.27.1.337
Wickham H, Chang W, Henry L, et al (2019) ggplot2: create elegant data visualisations using the grammar of graphics. R package version 3.3.3. https://CRAN.R-project.org/package=ggplot2
Wilby RL, Beven KJ, Reynard NS (2008) Climate change and fluvial flood risk in the UK: more of the same? Hydrol Process 22:2511–2523
Acknowledgements
We are grateful to the Brazilian National Council of Research and Development (CNPq) and the Coordination for the Improvement of Higher Education Personnel (CAPES) for financial support. C.C.B. and F.A.L.T. are grateful for the research productivity grant provided by CNPq. We thank Nupélia and PELD (site 6)/CNPq for logistic and financial support.
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Bomfim, F.F., Lansac-Tôha, F.M., Bonecker, C.C. et al. Determinants of zooplankton functional dissimilarity during years of El Niño and La Niña in floodplain shallow lakes. Aquat Sci 83, 41 (2021). https://doi.org/10.1007/s00027-021-00796-6
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DOI: https://doi.org/10.1007/s00027-021-00796-6