SYNERGISTIC EFFECTS OF NATURAL AND ANTHROPOGENIC IMPACTS ON ZOOPLANKTON DIVERSITY IN A SUBTROPICAL FLOODPLAIN: A LONG-TERM STUDY
DOI:
https://doi.org/10.4257/oeco.2020.2402.20Palavras-chave:
Biodiversity, damming effect, invasive species, large rivers, oligotrophication.Resumo
Large biological diversity can be observed in floodplains, which is linked to several ecosystem processes, such as productivity and nutrient cycling; among the species involved in these processes are zooplanktonic organisms. Here, we aimed to quantify the temporal trend of zooplankton, through changes in species richness and composition (β-diversity) and the abundance of individuals, in preserved and non-preserved sites of the Upper Paraná River floodplain during the last 19 years, and 617 species (321 rotifers, 135 testate amoebae, 107 cladocerans, and 54 copepods) were recorded. The highest species richness was verified in 2002 and the lowest in 2016. Zooplankton richness and abundance in non-preserved sites show clear temporal homogenization, while preserved sites show cyclical fluctuations over time. The rarefaction curve showed the biodiversity potential in this floodplain. Three invasive species were recorded (Kellicottia bostoniensis, Daphnia lumholtzi, and Mesocyclops ogunnos). The variation in the hydrologic regime, the oligotrophication, and the reduced connectivity among the sites were the main factors interfering in the species composition over the years and leading to a reduction of the species richness and abundance. The preservation of the tributaries with pristine characteristics is very important for the mitigation of these synergistic effects under the community structure.
Referências
Agostinho, A.A., Gomes, L.C. & Pelicice, F.M. 2007. Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. EDUEM, Maringá. p. 501.
Agostinho, A. A., Pelicice, F. M., & Gomes L. C. 2008. Dams the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology, 68(4), 1119–1132. DOI: 0.1590/S1519-69842008000500019
Agostinho, A. A., Pelicice, F. M., & Marques, E. E. 2009. Reservatório de peixe angical: bases ecológicas para o manejo da ictiofauna. São Carlos: RiMa: p. 188.
Allan, J. D. 1976. Life History Patterns in Zooplankton. The American Naturalist 110, 971, 165–180. DOI:10.1086/283056 39
Anderson, M. J., Ellingsen, K. E., & McArdle, B. H. 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 9(6), 683–693. DOI: 10.1111/j.14610248.2006.00926.x
Angeler, D., & Moreno, J. 2007. Zooplankton community resilience after press-type anthropogenic stress in temporary ponds. Ecological Applications, 17(4), 1105–1115. DOI: 10.1890 / 06-1040
Arrieira, R. L., Schwind, L. T. F., Bonecker, C. C., & Lansac-Tôha, F. A. 2015. Use of functional diversity to assess determinant assembly processes of testate amoebae community. Aquatic Ecology, 49, 561–571. DOI: 10.1007/s10452-015-9546-z
Auer, M. T., & Powell, K. D. 2004. Heterotrophic Bacterioplankton Dynamics at a Site off the Southern Shore of Lake Superior. Journal of Great Lakes Research, 30, 214–229. DOI: 10.1016/S0380-1330(04)70387-1 40
Bomfim, F.F., Mantovano, T., Amaral, D.C., Palhiarini, W.S., Bonecker, C.C. & Lansac-Tôha, F.A. 2017. Adjacent environments contribute to the increase of zooplankton species in a neotropical river. Acta Limnologica Brasiliensia, 29, 1–14.
Bonecker, C. C., Simões N. R., Minte-Vera, C. V., Lansac-Tôha, F. A., Velho, L. M., & Agostinho, A. A. 2013. Temporal changes in zooplankton species diversity in response to environmental changes in an alluvial valley. Limnologica, 43, 114–121. DOI: 10.1016/j.limno.2012.07.007
Bozelli, R. L., Thomaz, S.M., Padial, A. A., Lopes, P. M., & Bini, L. M. 2015. Floods decrease zooplankton beta diversity and environmental heterogeneity in an Amazonian floodplain system. Hydrobiologia, 753(1), 233–241. DOI: 10.1007/s10750-015-2209-1
Braghin, L. S. M., Almeida, B. D. A., Amaral, D. C., Canella, T. F., Garcia, B. C. G. & Bonecker, C. C. 2018. Effects of dams decrease zooplankton functional β-diversity in river-associated lakes. Freshwater Biology, 63, 121–130. DOI: 10.1111/fwb.13117.
Braghin, L. S., Figueiredo, B. R., Meurer, T., Michelan, T. S., Simões, N. R., & Bonecker, C. C. 2015. Zooplankton diversity in a dammed river basin is maintained by preserved tributaries in a tropical floodplain, Aquatic Ecology, 49(2), 175–187. DOI: 10.1007/s10452-015-9514-7.
Brito, M. T. da S., Heino, J., Pozzobom, U. M. & Landeiro, V. L. 2020. Ecological uniqueness and species richness of zooplankton in subtropical floodplain lakes. Aquatic Sciences, 82, 1–13.
Bunn, S. E., & Arthington, A. H. 2002. Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity. Environmental Management, 30(4), 492–507. DOI: 10.1007/s00267-002-2737-0
Buosi, P. R. B., Pauletto, G. M., Lansac-Tôha. F. A., & Velho, L. F. M. 2011. Ciliate community associated with aquatic macrophyte roots: effects of nutrient enrichment on the community composition and species richness. European Journal of Protistology, 47, 86–102. DOI: 10.1016/j.ejop.2011.02.001.
Cazzanelli, M., Warming, T. P., & Christoffersen, K. S. 2008. Emergent and floating-leaved macrophytes as refuge for zooplankton in a eutrophic temperate lake without submerged vegetation. Hydrobiologia, 605(1), 113–122. DOI: 10.1007/s10750-008-9324-1.
Chaparro G., Marinone, M. C., Lombardo, R., Schiaffino M. R., & Guimarães A. S. 2011. Zooplancton succession during extraordinary drought‐flood cycles. A case study in a South American floodplain lake. Limnologica, 41, 371–381. DOI: 10.1016/j.limno.2011.04.003
Crawley, M. J. 2007. The R book. Chichester, United Kingdom: Wiley. p. 1076.
Cunha, E. R., Thomaz, S. M., Mormul, R. P., Cafofo, E. G., & Bonaldo, A. B. 2012. Macrophyte Structural Complexity Influences Spider Assemblage Attributes in Wetlands. Wetlands 32, 369–377. DOI: 10.1007/s13157-012-0272-1
Fernandes, R., Agostinho, A. A., Ferreira, E. A., Pavanelli, C. S., Suzuki, H. I., Lima, D. P., & Gomes, L. C. 2009. Effects of the hydrological regime on the ichthyofauna of riverine environments of the Upper Paraná River floodplain. Brazilian Journal of Biology, 69, 669–680.
Field, R., Hawkins, B. A., Cornell, H. V., Currie, D. J., Diniz‐Filho, J. A. F., Guégan, J. F., Dawn M. Kaufman, D. M., Kerr, J. T., Mittelbach, G. G., Oberdorff, T. T., O’Brien, E. M. & John R. G. Turner. 2009. Spatial species‐richness gradients across scales: a meta‐analysis. Journal of biogeography, 36, 132–147. DOI: 10.1111/j.1365-2699.2008.01963.x
Franklin, J. F. 1989. Importance and justification of long-term studies in ecology. In: Long-term studies in ecology. Ed. by G. E. Likens. Springer, New York, 3–19.
Golterman, H. L., Clyno, R. S., & Ohnstad, M. A. M. 1978. Methods for physical and chemical analysis of freshwaters. 2nd ed. Blackwell, Oxford. p. 315.
Havel, J. E., Lee, C. E., & Zanden, J. V. 2005. Do reservoirs facilitate invasions into landscapes? BioScience, 55(6), 518–525. DOI: 10.1641/0006-3568(2005)055[0518:DRFIILorgeous2.0.CO;2
Hooper, D. U., Chapin, F. S., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeen, S., Schmid, B., Seta, L. A., Symstad, A. J., Vandermeer, J., & Wardle, D.A. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75(1), 3–35. DOI: 10.1890/04-0922
Jati, S., Bortolini, J. C., Moresco, G. A., Paula, A. C. M. D., Rodrigues, L. C., Iatskiu, P., Pineda, A., Zanco, B. F., da Silva, M. V., Souza, Y. R. 2017. Phytoplankton community in the last undammed stretch of the Paraná River: considerations on the distance from the dam. Acta Limnologica Brasiliensia, 29, e112.
Junk, W. J., Bayley, P. B., & Sparks, R. E. 1989. The flood pulse concept in river-floodplain systems. Canadian special publication of fisheries and aquatic sciences, 106(1), 110–127.
Kovalenko, K. E., Thomaz, S. M., & Warfe, D. M. 2012. Habitat complexity: approaches and future directions. Hydrobiologia, 685, 1–17. DOI: 10.1007/s10750-011-0974-z
Lansac-Tôha, F. A., Bonecker, C. C., Velho, L. F. M., Simões, N. R., Dias, J. D., Alves, G. M., & Takahasi, E. M. 2009. Biodiversity of zooplankton communities in the Upper Paraná River floodplain: interannual variation from long-term studies. Brazilian Journal of Biology, 69(2), 539–549. DOI: 10.1590/S1519-69842009000300009
Lansac-Tôha, F. A., Velho, L. F. M., & Bonecker, C. C. 2003. Influência de macrófitas aquáticas sobre a estrutura da comunidade zooplanctônica. In: Thomaz, S. M. and Bini, L. M. (Eds.). Ecologia e Manejo de Macrófitas Aquáticas. pp. 231–242. Maringá: Eduem.
Lansac-Tôha, F. A., Velho, L. F. M., Higuti, J., & Takahashi, E. M. 2002. Cyclopidae (Crustacea, Copepoda) from the upper Paraná River floodplain, Brazil. Brazilian Journal of Biology, 62(1), 125–133. DOI: 10.1590/S1519-69842002000100015
Larsen, S., Karaus, U., Claret, C., Sporka, F., Hamerlík, L., Tockner, K. 2019. Flooding and hydrologic connectivity modulate community assembly in a dynamic river-floodplain ecosystem. PLoS ONE, 14, 1–22.
Loreau, M. 2000. Biodiversity and ecosystem functioning: recent theoretical advances. Oikos, 91(1), 3–17. DOI: 10.1034/j.1600-0706.2000.910101.x
Mace, G. M. 2010. Drivers of biodiversity change. In: Leader-Williams, N., Adams, W. M. & Smith, R. J. (Eds.). Trade-offs in conservation: deciding what to save. pp. 349–364. Wiley Blackwell, Oxford.
Mack, R. N., Simberloff D., Lonsdale, W. M., Evans, H., Clout, M. & Bazzaz, F. 2000. Biotic Invasions: causes, epidemiology, global consequences and control. Ecology, 10(3), 689–710. DOI: 10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2.
Magurran, A. E. & Dornellas, M. 2010. Biological diversity in a changing world. The Royal Society, 365, 3593–3597. DOI: 10.1098/rstb.2010.0296 38.
Meerhoff, M., Iglesias, C., De Mello, F. T., Clemente, J., Jensen, E., Lauridsen, T. L., & Jeppesen, E. 2007. Effects of habitat complexity on community structure and predator avoidance behavior of littoral zooplankton in temperate versus subtropical shallow lakes. Freshwater Biology, 52(6), 1009–1021. https://doi.org/10.1111/j.1365-2427.2007.01748.x
Meurer, M., Martins, D. P., & Souza Filho, E. E. 2005. Dinâmica das vazões reguladas pelas usinas de Porto Primavera e Rosana, na região do Pontal do Paranapanema, no período 1999-2003. Geosul 20 (40): 147–166.
Mormul, R. P., Ahlgren, J., Ekvall, K. M., Hansson, L-A., & Brönmark, C. 2012. Water brownification may increase the invasibility of a submerged non-native macrophyte. Biological Invasions, 14(10), 1–9. DOI: 10.1007/s10530-012-0216-y
Neiff, J. J. 1990. Ideas para la interpretacion ecologica del Parana. Interciencia, 15(6), 424–441. DOI: 0378-1844/90/06-424-18
Oksanen. J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E. & Wagner E. 2018. vegan: Community Ecology Package. R package version 2.5-3.https://CRAN.R-project.org/package=vegan
Opperman, J. J., Luster R., McKenney, B. A., & Meadows, A. W. 2010. Ecologically Functional Floodplains: Connectivity, Flow Regime, and Scale. Journal of the American Water Resources Association (JAWRA), 46(2), 211–226. DOI:10.1111/j.1752-1688.2010.00426.x.
Ovaskainen, O., Weigel, B., Potyutko, O. & Buyvolov, Y. 2019 Long-term shifts in water quality show scale-dependent bioindicator responses across Russia – Insights from 40 year-long bioindicator monitoring program. Ecological Indicators, 98, 476–482. DOI: 10.1016/j.ecolind.2018.11.027.
Padovesi-Fonseca, C., & Rezende, R. D. S. 2017. Factors that drive zooplankton diversity in Neo-Tropical Savannah shallow lakes. Acta Limnologica Brasiliensia, 29, e15. DOI: 10.1590/s2179-975x1817
Pinheiro J, Bates D, DebRoy, S., &Sarkar,D, R Core Team (2020). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-145, https://CRAN.R-project.org/package=nlme.
R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Roberto, M. C., Santana, N. F., & Thomaz, S. M. 2009. Limnology in the upper Paraná River floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Brazilian Journal of Biology, 69(2), 717–725. DOI: 10.1590/S1519-69842009000300025. PMid:19738977.
Robertson, B. A., & Hardy, E. R. 1984. Zooplankton of Amazonian lakes and Rivers. In Sioli, H. (Ed.). The Amazon: limnology and landscape ecology of a might tropical river and its basin. pp. 337–352. Dordrecht: Junk Publishers.
Rodrigues, E. H. C., Barreto, L. N., Ferreira-Correia, M. M., & Silva, M. R. C. 2015. Variação temporal do fitoplâncton em um rio tropical pré-amazônico (Rio Pindaré, Maranhão, Brasil). Ciência e Natura, 37(2), 241–251. DOI: 10.5902/2179460X14855
Rodrigues, L. C., Pivato, B. M., Vieira, L. C. G., Bovo-Scomparin, V. M., Bortolini, J. C., Pineda, A., & Train, S. 2018. Use of phytoplankton functional groups as a model of spatial and temporal patterns in reservoirs: a case study in a reservoir of central Brazil. Hydrobiologia, 805(1), 147–161. DOI: 10.1007/s10750-017-3289-x
Rodrigues, L. C., Train, S., Bovo-Scomparin, V. M., Jati, S., Borsalli, C. C. J., & Marengoni, E. 2009. Interannual variability of phytoplankton in the main rivers of the Upper Paraná River floodplain, Brazil: influence of upstream reservoirs. Brazilian Journal of Biology, 69(2), 501–516. DOI: 10.1590/S1519-69842009000300006
Santana, N. F., Pereira, L. S., Roberto, M. D. C., Gomes, S. E. D. A., Pagioro, T. A., & Mormul, R. P. 2017. Longitudinal gradient in limnological variables in the Upper Paraná River: a brief description and the importance of undammed tributaries. Acta Limnologica Brasiliensia, 29, e116. DOI: 10.1590/s2179-975x0217.
Segers, H. 2008. Global diversity of rotifers (Rotifera) in freshwater. In Freshwater Animal Diversity Assessment. Springer, Dordrecht, 595, 49–59. DOI: 10.1007/s10750-007-9003-7
Serafim, J. R. M., Bonecker, C. C., Rossa, D. C., Lansac-Tôha, F. A. & Costa, C. L. 2003. Rotifers of the upper Paraná River floodplain: additions to the checklist. Brazilian Journal of Biology, 63(2), 207–212. DOI: 10.1590/S1519-69842003000200005
Sharma, B. K. 2005. Rotifer communities of floodplain lakes of the Brahmaputra basin of lower Assam (N.E. India): biodiversity, distribution and ecology. Hydrobiologia, 533(1-3), 209–221. DOI: 10.1007/s10750-004-2489-3.
Simões, N. R., Nunes, A.H., Dias, J. D., Lansac-Tôha, F. A., Velho, L. F. M., & Boecker, C.C. 2015. Impact of reservoirs on zooplankton diversity and implications for the conservation of natural aquatic environments. Hydrobiologia, 758, 3–17. DOI 10.1007/s10750-015-2260-y
Simões, N. R., Lansac-Tôha, F. A., Velho, L. F. M., & Bonecker, C. C. 2012. Intra and inter-annual structure of zooplankton communities in floodplain lakes: a long-term ecological research study. Revista de Biologia Tropical, 60(4), 1819–1836. DOI: 10.15517/rbt.v60i4.2183.
Simões, N. R., Robertson, B. A., Lansac-Tôha, F. A., Takahashi, E. M., Bonecker, C. C., Velho, L. F. M., & Joko, C. Y. 2009. Exotic species of zooplankton in the upper Paraná river floodplain, Daphnia lumholtzi Sars, 1885 (Crustacea: Branchiopoda). Brazilian Journal of Biology, 69(2), 551–558. DOI: 10.1590/S1519-69842009000300010.
Souza Filho, E. E. 2009. Evaluation of the Upper Paraná River discharge controlled by reservoirs. Brazilian Journal of Biology, 69(2), 707–716. DOI: 10.1590/S1519-69842009000300024.
Thomaz, S. M., Bini, M. L., & Bozelli, R. L. 2007. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia, 579(1), 1–13 DOI: 10.1007/s10750-006-0285-y.
Thomaz, S. M., Pagioro, T. A., Bini, L. M., Roberto, M. C., & Rocha, R. R. A. 2004. Limnological characterization of the aquatic environments and the influence of hydrometric levels. In Thomaz, S. M., Agostinho, A. A. and Hahn, N. S. (Eds.). The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. pp. 75–102. Leiden: Backhuys Publishers.
Train, S., & Rodrigues, L. C. 2004. Phytoplankton assemblages. The Upper Paraná river floodplain: physical aspects, ecology and conservation. Netherlands: Backhuys, 103–124.
Van der Valk, A. G. 2012. The biology of freshwater wetlands. Oxford University Press. 2nd ed. p. 296.
Ward, J. V., & Tockner, K. 2001. Biodiversity: towards a unifying theme for river ecology. Freshwater Biology, 46(2), 807–819. DOI: 10.1046/j.1365-2427.2001.00713.x
Wickham, H. (2016). ggplot2: elegant graphics for data analysis. Springer. p. 213.
Winemiller, K. O., Mcintyre, P. B., Castello, L., Fluet-chouinard, E., Giarrizzo, T., Nam, S., Baird, I. G., Darwall, W., Lujan, N. K., Harrison, I., Stiassny, M. L. J., Silvano, R. A. M., Fitzgerald, D.B., Pelicice, F. M., Agostinho, A. A., Gomes, L. C., Albert, J. S., Baran, E., Petrere Junior, M., Zarfl, C., Mulligan, M., Sullivan, J. P., Arantes, C. C., Sousa, L. M., Koning, A. A., Hoeinghaus, D. J., Sabaj, M., Lundberg, J. G., Armbruster, J., Thieme, M. L., Petry, P., Zuanon, J., Vilara, G. T., Snoeks, J., Ou, C., Rainboth, W., Pavanelli, C. S., Akama, A., Soesbergen, A., & Saenz, L. 2016. Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science, 351(6269), 128–129. PMid:26744397. DOI: 10.1126/science.aac7082.
Wood, S.N. 2017. Generalized Additive Models: An Introduction with R, 2nd ed. Boca Raton, FL: CRC Press. p. 496. DOI: 10.1201/9781315370279
Wood, S. N. 2006. Generalized Additive Models: An Introduction with R. Chapman & Hall/CRC. p. 410.
