Acta Limnologica Brasiliensia
https://www.actalb.org/article/doi/10.1590/S2179-975X7823
Acta Limnologica Brasiliensia
Original Article

Rainfall increases the biomass and drives the taxonomic and morpho-functional groups variability of phytoplankton in a subtropical urban lake

A pluviosidade aumenta a biomassa e impulsiona a variabilidade dos grupos taxonômicos e morfo-funcionais do fitoplâncton em um lago urbano subtropical

Matheus Vieira da Silva; Susicley Jati

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Abstract

Aim: To explore the short-term effects of rainfall events on the biomass, density, and richness of the phytoplankton community during dry and rainy periods, as well as on the selection and response of Morphology-Based Functional Groups (MBFG).

Methods: The phytoplankton community and abiotic environmental variables were sampled over a short period in a subtropical urban lake during the dry and rainy seasons (2018-2019). Generalized Linear Models (GLMs) were generated to analyze the relationship between phytoplankton biovolume, density, and richness with abiotic variables. The predictability of phytoplankton functional groups was assessed using Redundancy Analysis (RDA).

Results: There was an increase in the density and biovolume of the phytoplankton community during the rainy period. Species richness decreased with increased rainfall. The lake exhibited a high dominance of Cyanobacteria (MBFG VIII), mainly represented by Raphidiopsis raciborskii (Woloszynska) Aguilera in both periods studied.

Conclusions: We found evidence supporting the hypothesis that rainfall events increase the density and biovolume of phytoplankton. Morphology-based functional groups served as efficient indicators of the lake's environmental conditions.

Keywords

ammonium, cyanobacteria, meteorological factors, precipitation

Resumo

Objetivo: Explorar os efeitos a curto prazo de eventos de chuva na biomassa, densidade e riqueza da comunidade fitoplanctônica durante os períodos seco e chuvoso, bem como na seleção e resposta de Grupos Funcionais Baseados na Morfologia (MBFG).

Métodos: A comunidade fitoplanctônica e as variáveis ambientais abióticas foram amostradas em um curto período em um lago urbano subtropical durante as estações seca e chuvosa (2018-2019). Modelos Lineares Generalizados (GLMs) foram gerados para analisar a relação entre o biovolume, a densidade e a riqueza do fitoplâncton com as variáveis abióticas. A previsibilidade dos grupos funcionais de fitoplâncton foi avaliada usando Análise de Redundância (RDA).

Resultados: Houve um aumento da densidade e do biovolume da comunidade fitoplanctônica no período chuvoso. A riqueza de espécies diminuiu com o aumento da pluviosidade. O lago exibiu uma alta dominância de Cyanobacteria (MBFG VIII), principalmente representadas por Raphidiopsis raciborskii (Woloszynska) Aguilera nos dois períodos estudados.

Conclusões: Encontramos evidências que sustentam a hipótese de que eventos de chuva aumentam a densidade e o biovolume do fitoplâncton. Os grupos funcionais baseados na morfologia serviram como indicadores eficientes das condições ambientais do lago.

Palavras-chave

amônia, cyanobacteria, fatores meteorológicos, precipitação

References

Almanza-Marroquín, V., Figueroa, R., Parra, O., Fernández, X., Baeza, C., Yañez, J., & Urrutia, R., 2016. Bases limnológicas para la gestión de los lagos urbanos de Concepción, Chile. Lat. Am. J. Aquat. Res. 44(2), 313-326. http://doi.org/10.3856/vol44-issue2-fulltext-12.

American Public Health Association - APHA, & American Water Works Association, 1995. Standard methods for the examination of water and wastewater. USA: APHA.

Aubriot, L., & Bonilla, S., 2018. Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N: P ratios. Freshw. Biol. 63(3), 318-329. http://doi.org/10.1111/fwb.13066.

Aubriot, L., 2019. Nitrogen availability facilitates phosphorus acquisition by bloom-forming cyanobacteria. Microb. Ecol. 95(2), 229. PMid:30476121. http://doi.org/10.1093/femsec/fiy229.

Austin, M., 1999. The potential contribution of vegetation ecology to biodiversity research. Ecography 22(5), 465-484. http://doi.org/10.1111/j.1600-0587.1999.tb01276.x.

B-Béres, V., Naselli-Flores, L., Padisák, J., & Borics, G., 2024. Trait-based ecology of microalgae. Hydrobiologia 851, 713-732. https://doi.org/10.1007/s10750-023-05465-3.

Baselga, A., & Orme, C.D.L., 2012. betapart: an R package for the study of beta diversity. Methods Ecol. Evol. 3(5), 808-812. http://doi.org/10.1111/j.2041-210X.2012.00224.x.

Bhagowati, B., & Ahamad, K.U., 2019. A review on lake eutrophication dynamics and recent developments in lake modeling. Ecohydrol. Hydrobiol. 19(1), 155-166. http://doi.org/10.1016/j.ecohyd.2018.03.002.

Bittencourt-Oliveira, M.C., Dias, S.N., Moura, A.N., Cordeiro-Araújo, M.K., & Dantas, E.W., 2012. Dinâmica sazonal de cianobactérias em um reservatório eutrófico (Arcoverde) no semiárido brasileiro. Braz. J. Biol. 72, 533-544. PMid:22990824. http://doi.org/10.1590/S1519-69842012000300016.

Boccard, D., Gillet, F., & Legendre, P., 2011. Numerical ecology with R. New York: Springer. http://doi.org/10.1007/978-1-4419-7976-6.

Borges, P.A.F., Train, S., & Rodrigues, L.C., 2008. Estrutura do fitoplâncton, em curto período de tempo, em um braço do reservatório de Rosana (Ribeirão do Corvo, Paraná, Brasil. Acta Sci. Biol. Sci. 30(1), 57-65.

Bortolini, J.C., & Bueno, N.C., 2017. Temporal dynamics of phytoplankton using the morphology-based functional approach in a subtropical river. Rev. Bras. Bot. Braz. J. Bot. 40(3), 741-748. http://doi.org/10.1007/s40415-017-0385-0.

Bovo M.C. & Amorim M.C.C.T., 2009. Áreas Verdes Urbanas, a Imagem, o Mito e a Realidade: um estudo de caso sobre a cidade de Maringá/PR/BR. Formação (Online), 1(16), 60-69. https://doi.org/10.33081/formacao.v1i16.865.

Boyd, C.E., 2021. Eutrophication. In: Boyd, C.E. Water quality: an introduction. Springer Nature, 311-322. https://doi.org/10.1007/978-3-030-23335-8_15.

Brasil. Conselho Nacional do Meio Ambiente, 18 mar 2005. Resolução nº 357. Diário Oficial da União [da] República Federativa do Brasil, Poder Executivo, Brasília, DF.

Butterwick, C., Heaney, S.I., & Talling, J.F., 2005. Diversityin the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw. Biol. 50(2), 291-300. http://doi.org/10.1111/j.1365-2427.2004.01317.x.

Calcagno, V., & Mazancourt, C., 2010. glmulti: an R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. 34(12), 1-29. http://doi.org/10.18637/jss.v034.i12.

Calijuri, M.C., Alves, M.A.S., & Santos, A.C.A., 2006. Cianobartérias e cianotoxinas em águas continentais. São Carlos: Rima.

Carrick, H., Cafferty, E., Ilacqua, A., Pothoven, S., & Fahnenstiel, G., 2017. Seasonal abundance, biomass and morphological diversity of picoplankton in Lake Superior: importance of water column mixing. Inter. J. Hydrol. 1(6), 187-197. http://doi.org/10.15406/ijh.2017.01.00034.

Catherine, A., Selma, M., Mouillot, D., Troussellier, M., & Bernard, C., 2016. Patterns and multi-scale drivers of phytoplankton species richness in temperate peri-urban lakes. Sci. Total Environ. 559, 74-83. PMid:27054495. http://doi.org/10.1016/j.scitotenv.2016.03.179.

Chen, Q., Huang, M., & Tang, X., 2020. Eutrophication assessment of seasonal urban lakes in China Yangtze River Basin using Landsat 8-derived Forel-Ule index: a six-year (2013–2018) observation. Sci. Total Environ. 745, 135392. PMid:31892484. http://doi.org/10.1016/j.scitotenv.2019.135392.

Cole, G., 1994. Textbook of limnology. 4th ed. Illinois: Waveland Press.

Cunha, D.G.F., do Carmo, C.M., & Lamparelli, M.C., 2013. A trophic state index for tropical/subtropical reservoirs (TSItsr). Ecological Engineering 60, 126-134.

Cupertino, A., Gücker, B., Von Rückert, G., & Figueredo, C.C., 2019. Phytoplankton assemblage composition as an environmental indicator in routine lentic monitoring: taxonomic versus functional groups. Ecol. Indic. 101, 522-532. http://doi.org/10.1016/j.ecolind.2019.01.054.

Dantas, Ê.W., Bittencourt-Oliveira, M.D.C., & Moura, A.D.N., 2010. Spatial-temporal variation in coiled and straight morphotypes of Cylindrospermopsis raciborskii (Wolsz) Seenayya et Subba Raju (Cyanobacteria). Acta Bot. Bras. 24(2), 585-591. http://doi.org/10.1590/S0102-33062010000200028.

Dixon, P., 2003. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14(6), 927-930. http://doi.org/10.1111/j.1654-1103.2003.tb02228.x.

Domingues, R.B., Barbosa, A.B., Sommer, U., & Galvão, H.M., 2011. Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquat. Sci. 73(3), 331-343. http://doi.org/10.1007/s00027-011-0180-0.

Elliott, J.A., 2010. The seasonal sensitivity of cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Glob. Change Biol. 16(2), 864-876. http://doi.org/10.1111/j.1365-2486.2009.01998.x.

Fabrin, T.M.C., Stabile, B.H.M., Silva, M.V., Jati, S., Rodrigues, L., & de Oliveira, A.V., 2020. Cyanobacteria in an urban lake: hidden diversity revealed by metabarcoding. Aquat. Ecol. 54(2), 671-675. http://doi.org/10.1007/s10452-020-09763-z.

Ferrão-Filho, A.S., Domingos, P., & Azevedo, S.M., 2002. Influences of a Microcystis aeruginosa Kützing bloom on zooplankton populations in Jacarepaguá Lagoon (Rio de Janeiro, Brazil). Limnologica 32(4), 295-308. http://doi.org/10.1016/S0075-9511(02)80021-4.

Fialkowska, E., & Pajdak-Stós, A., 2002. Dependence of cyanobacteria defense mode on grazer pressure. Aquat. Microb. Ecol. 27(2), 149-157.

Figueiredo, C.C., & Giani, A., 2009. Phytoplankton community in the tropical lake of Lagoa Santa (Brazil): conditions favoring a persistent bloom of Raphidiopsis raciborskii. Limnologica 39(4), 264-272. http://doi.org/10.1016/j.limno.2009.06.009.

Gamelgo, M.C.P., Mucci, J.L.N., & Navas-Pereira, D., 2009. Population dynamics: seasonal variation of phytoplankton functional groups in Brazilian reservoirs (Billings and Guarapiranga, São Paulo. Braz. J. Biol. 69(4), 1001-1013. PMid:19967171. http://doi.org/10.1590/S1519-69842009000500004.

Gao, Y., Deng, Z., & Morrison, A.M., 2019. Can urban lake recreational pressure be measured? The impacts of urbanization on Wuhan’s Lakes. Appl. Spat. Anal. Policy 12(2), 255-273. http://doi.org/10.1007/s12061-017-9241-7.

Gentil, R.C., Tucci, A., & Sant’Anna, C.L., 2008. Dinâmica da comunidade fitoplanctônica e aspectos sanitários de um lago urbano eutrófico em São Paulo, SP. Hoehnea 35(2), 265-280. http://doi.org/10.1590/S2236-89062008000200008.

Ghadouani, A., Pinel‐Alloul, B., & Prepas, E.E., 2003. Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshw. Biol. 48(2), 363-381. http://doi.org/10.1046/j.1365-2427.2003.01010.x.

Golterman, H.L., Clymo, R.S., & Ohnstad, M.A.M., 1978. Methods for physical and chemical analysis of freshwater. Oxford: Blackwell Scientific Publication, 2nd ed.

Huisman, J., Codd, G.A., Paerl, H.W., Ibelings, B.W., Verspagen, J.M., & Visser, P.M., 2018. Cyanobacterial blooms. Nat. Rev. Microbiol. 16(8), 471-483. PMid:29946124. http://doi.org/10.1038/s41579-018-0040-1.

Huszar, V.L.M., Silva, L.H.S., Marinho, M., Domingos, P., & Sant’Anna, C.L., 2000. Cyanoprokaryote assemblages in eight productive tropical Brazilian waters. Hydrobiologia 424(1), 67-77. http://doi.org/10.1023/A:1003996710416.

Jati, S., 2019. Revisão do Plano de Manejo do Parque do Ingá: Condições limnológicas e vegetação terrestre. Biblioteca Setorial do Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura. Maringá: NUPELIA- Universidade Estadual de Maringá, vol. 1.

Jati, S., Bortolini, J.C., Moresco, G.A., Paula, A.C.M.D., Rodrigues, L.C., Iatskiu, P., & Silva, M.V., 2017. Phytoplankton community in the last undammed stretch of the Paraná River: considerations on the distance from the dam. Acta Limn. Bras., 29, e112. https://doi.org/10.1590/S2179-975X4017.

Kassambara, A., & Mundt, F., 2020. Factoextra: extract and visualize the results of multivariate data analyses. R package, v.1. [online]. Retrieved in 2023, August 21, from https://CRAN.R-project.org/package=factoextrahttps://www.R-project.org/.

Kruk, C., Devercelli, M., & Huszar, V.L., 2021. Reynolds functional groups: a trait-based pathway from patterns to predictions. Hydrobiologia 848(1), 113-129. http://doi.org/10.1007/s10750-020-04340-9.

Kruk, C., Huszar, V.L., Peeters, E.T., Bonilla, S., Costa, L., Lürling, M., & Scheffer, M., 2010. A morphological classification capturing functional variation in phytoplankton. Freshw. Biol. 55(3), 614-627. http://doi.org/10.1111/j.1365-2427.2009.02298.x.

Le Moal, M., Gascuel-Odoux, C., Ménesguen, A., Souchon, Y., Étrillard, C., Levain, A., Moatar, F., Pannard, A., Souchu, P., Lefebvre, A., & Pinay, G., 2019. Eutrophication: a new wine in an old bottle? Sci. Total Environ. 651(Pt 1), 1-11. PMid:30223216. http://doi.org/10.1016/j.scitotenv.2018.09.139.

Lê, S., Josse, J., & Husson, F., 2008. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25(1), 1-18. http://doi.org/10.18637/jss.v025.i01.

Legendre P. & Legendre L., 1998. Numerical ecology (Developments in Environmental Modelling). USA: Elsevier, vol. 20.

Li, D., Wu, N., Tang, S., Su, G., Li, X., Zhang, Y., & Giesy, J., 2018. Factors associated with blooms of cyanobacteria in a large shallow lake, China. Environ. Sci. Eur. 30(1), 27. PMid:30148024. http://doi.org/10.1186/s12302-018-0152-2.

Li, X., Huo, S., Zhang, J., Xiao, Z., Xi, B., & Li, R., 2020. Factors related to aggravated Raphidiopsis (Cyanobacteria) bloom following sediment dredging in an eutrophic shallow lake. Environ. Sci. Ecotechnology 100014, 100014. PMid:36160924. http://doi.org/10.1016/j.ese.2020.100014.

Li, Y., Shang, J., Zhang, C., Zhang, W., Niu, L., Wang, L., & Zhang, H., 2021. The role of freshwater eutrophication in greenhouse gas emissions: a review. Sci. Total Environ. 768, 144582. PMid:33736331. http://doi.org/10.1016/j.scitotenv.2020.144582.

Lund, J.W.G., Kipling, C., & Le Cren, E.D., 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11, 143-170.

Lv, J., Wu, H., & Chen, M., 2011. Effects of nitrogen and phosphorus on phytoplankton composition and biomass in 15 subtropical, urban shallow lakes in Wuhan, China. Limnologica 41(1), 48-56. http://doi.org/10.1016/j.limno.2010.03.003.

Maack, R., 1981. Geografia física do Estado do Paraná. Rio de Janeiro: Livraria José Olympio Editora.

Mackereth, F.Y.H., Heron, J.R., & Tailing, J.F., 1978. Water analysis: some revised methods for limnologists. Sci. Publ. Freshw. Biol. Assoc.

Margalef, R., 1983. Limnologia. Barcelona: Omega.

Maruya, Y., Nakayama, K., Sasaki, M., & Komai, K., 2023. Effect of dissolved oxygen on methane production from bottom sediment in a eutrophic stratified lake. J. Environ. Sci. (China) 125, 61-72. PMid:36375943. http://doi.org/10.1016/j.jes.2022.01.025.

Meira, B.R., Lansac-Tôha, F.M., Segovia, B.T., Oliveira, F.R., Buosi, P.R.B., Jati, S., Rodrigues, L.C., Lansac-Tôha, F.A., & Machado-Velho, L.F., 2017. Abundance and size structure of planktonic protist communities in a Neotropical floodplain: effects of top-down and bottom-up controls. Acta Limn. Bras., 29, e104. https://doi.org/10.1590/S2179-975X6117.

Mittelbach, G.G., Steiner, C.F., Scheiner, S.M., Gross, K.L., Reynolds, H.L., Waide, R.B., Willig, M.R., Dodson, S.I., & Gough, L., 2001. What is the observed relationship between species richness and productivity? Ecology 82(9), 2381-2396. http://doi.org/10.1890/0012-9658(2001)082[2381:WITORB]2.0.CO;2.

Moraes, L.A.F., 2009. A visão integrada da ecohidrologia para o manejo sustentável dos ecossistemas aquáticos. Oecol. Aust. 13(4), 676-687. http://doi.org/10.4257/oeco.2009.1304.11.

Nabout, J.C., & Nogueira, I.D.S., 2011. Variação temporal da comunidade fitoplanctônica em lagos urbanos eutróficos. Acta Sci. Biol. Sci. 33(4), 383-391. http://doi.org/10.4025/actascibiolsci.v33i4.5955.

Naselli-Flores, L., 2008. Urban lakes: ecosystems at risk, worthy of the best care. In Proceedings of Taal 2007: the 12th world lake conference (Vol. 1333, p. 1337). India: Ministry of Environment, Government of India..

Nardini, M.J., & Nogueira, I.D.S., 2008. O processo antrópico de um lago artificial e o desenvolvimento da eutrofização e florações de algas azuis em Goiânia. Rev. Est 35(2), 23-52.

Naselli-Flores, L., Padisák, J., & Albay, M., 2007. Shape and size in phytoplankton ecology: do they matter? Hydrobiologia 578(1), 157-161. http://doi.org/10.1007/s10750-006-2815-z.

Padisák, J., Crossetti, L.O., & Naselli-Flores, L., 2009. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621(1), 1-19. http://doi.org/10.1007/s10750-008-9645-0.

Panosso, R., Carlsson, P.E.R., Kozlowsky-Suzuki, B., Azevedo, S.M., & Granéli, E., 2003. Effect of grazing by a neotropical copepod, Notodiaptomus, on a natural cyanobacterial assemblage and on toxic and non-toxic cyanobacterial strains. J. Plankton Res. 25(9), 1169-1175. http://doi.org/10.1093/plankt/25.9.1169.

Perbiche-Neves, G., Ferreira, R.A.R., & Nogueira, M.G., 2011. Phytoplankton structure in two contrasting cascade reservoirs (Paranapanema River, Southeast Brazil). Biologia (Bratisl.) 66(6), 967-982. http://doi.org/10.2478/s11756-011-0107-1.

Qin, B., Paerl, H.W., Brookes, J.D., Liu, J., Jeppesen, E., Zhu, G., & Deng, J., 2019. Why Lake Taihu continues to be plagued with cyanobacterial blooms through 10 years (2007–2017) efforts. Sci. Bull. (Beijing) 64(6), 354-356. PMid:36659719. http://doi.org/10.1016/j.scib.2019.02.008.

R Core Team, 2023. A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing [online]. Retrieved in 2023, August 21, from https://www.R-project.org/.

Reynolds, C.S. 2006. Ecology of phytoplankton. Cambrigde: Cambrigde University Press. http://doi.org/10.1017/CBO9780511542145.

Reynolds, C.S., Elliott, J.A., & Frassl, M.A., 2014. Predictive utility of trait-separated phytoplankton groups: a robust approach to modeling population dynamics. J. Great Lakes Res. 40, 143-150. http://doi.org/10.1016/j.jglr.2014.02.005.

Richardson, J., Feuchtmayr, H., Miller, C., Hunter, P.D., Maberly, S.C., & Carvalho, L., 2019. Response of cyanobacteria and phytoplankton abundance to warming, extreme rainfall events and nutrient enrichment. Glob. Change Biol. 25(10), 3365-3380. PMid:31095834. http://doi.org/10.1111/gcb.14701.

Saker, M.L., Neilan, B.A., & Griffiths, D.J., 1999. Two morphological forms of Raphidiopsis raciborskii (Cyanobacteria) isolated from Solomon Dam, Palm Island, Queensland. J. Phycol. 35(3), 599-606. http://doi.org/10.1046/j.1529-8817.1999.3530599.x.

Santos, A.O., 2003. Caracterização do reservatório no Parque do Ingá, em Maringá-PR no que diz respeito a seus aspectos limnológicos [Dissertação de Mestrado em Geografia]. Maringá: Universidade Estadual de Maringá.

Shafik, H.M., 2003. Morfological characteristics of Cylindrospermopsis raciborskii (Wol.) See. Et Subba Raju in laboratory cultures. Acta Biol. Hung. 54(1), 121-136. PMid:12705328. http://doi.org/10.1556/ABiol.54.2003.1.13.

Silva, M.V., Bortolini, J.C., & Jati, S., 2022. The phytoplankton community as a descriptor of environmental variability: a case study in five reservoirs of the Paraná River basin. Acta Limn. Bras. 34, e1. https://doi.org/10.1590/S2179-975X4621.

Somdee, T., Kaewsan, T., & Somdee, A., 2013. Monitoring toxic cyanobacteria and cyanotoxins (microcystins and cylindrospermopsins) in four recreational reservoirs (Khon Kaen, Thailand). Environ. Monit. Assess. 185(11), 9521-9529. PMid:23715735. http://doi.org/10.1007/s10661-013-3270-8.

Søndergaard, M., Lauridsen, T.L., Johansson, L.S., & Jeppesen, E., 2017. Nitrogen or phosphorus limitation in lakes and its impact on phytoplankton biomass and submerged macrophyte cover. Hydrobiologia 795(1), 35-48. http://doi.org/10.1007/s10750-017-3110-x.

Stela, L.V., Ribeiro, K.F., & Crossetti, L.O., 2024. Functional and taxonomic approaches differently highlight local and spatial processes in phytoplankton metacommunities. Hydrobiologia 851(4), 785-800. http://doi.org/10.1007/s10750-023-05374-5.

Sun, J., & Liu, D., 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. J. Plankton Res. 25(2), 1331-1346. http://doi.org/10.1093/plankt/fbg096.

Train, S., Jati, S., Rodrigues, L.C., & Pivato, B.M., 2005. Distribuição espacial e temporal do fitoplâncton em três reservatórios da Bacia do Rio Paraná. In: Rodrigues, L., Thomaz, S.M., Agostinho, A.A., Gomes, L.C. Biocenoses em reservatórios: padrões espaciais e temporais. São Carlos: RiMa, 73-85.

Tucci, A., Sant’Anna, C.L., Gentil, R.C., & Azevedo, M.D.P., 2006. Fitoplâncton do Lago das Garças, São Paulo, Brasil: um reservatório urbano eutrófico. Hoehnea 33(2), 147-175.

Tundisi, J.G., & Tundisi, T.M., 2012. Limnology. Boca Raton: CRC Press. http://doi.org/10.1201/b11386.

Utermöhl, H., 1958. Zur vervollkommnung der quantitativen phytoplankton-methodik: mit 1 Tabelle und 15 abbildungen im Text und auf 1 Tafel. Internationale Vereinigung für theoretische und angewandte Limnologie. Mitteilungen 9(1), 1-38.

Van Dam, B.R., Tobias, C., Holbach, A., Paerl, H.W., & Zhu, G., 2018. CO2 limited conditions favor cyanobacteria in a hypereutrophic lake: an empirical and theoretical stable isotope study. Limnol. Oceanogr. 63(4), 1643-1659. http://doi.org/10.1002/lno.10798.

Vaz, S.R., Lenzi, E., Luchese, E.B., & Fávero, L.O.B., 1998. Dinâmica do chumbo no lago do Parque do Ingá, Maringá, PR, Brasil. Braz. Arch. Biol. Technol. 41(4), 457-466. http://doi.org/10.1590/S1516-89131998000400010.

Veerman, J., Kumar, A., & Mishra, D.R., 2022. Exceptional landscape-wide cyanobacteria bloom in Okavango Delta, Botswana in 2020 coincided with a mass elephant die-off event. Harmful Algae 111, 102145. PMid:35016759. http://doi.org/10.1016/j.hal.2021.102145.

Viana, R.B., Cavalcante, R.M., Braga, F.M.G., Viana, A.B., Araújo, J.C., Nascimento, R.F., & Pimentel, A.S., 2009. Risk assessment of trihalomethanes from tap water in Fortaleza, Brazil. Environ. Monit. Assess. 151(1-4), 317-325. PMid:18365760. http://doi.org/10.1007/s10661-008-0273-y.

Violle, C., Navas, M.L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., & Garnier, E., 2007. Letthe concept of trait be functional! Oikos 116(5), 882-892. http://doi.org/10.1111/j.0030-1299.2007.15559.x.

Weber, S.J., Mishra, D.R., Wilde, S.B., & Kramer, E., 2020. Risks for cyanobacterial harmful algal blooms due to land management and climate interactions. Sci. Total Environ. 703, 134608. PMid:31757537. http://doi.org/10.1016/j.scitotenv.2019.134608.

Weisse, T., Gröschl, B., & Bergkemper, V., 2016. Phytoplankton response to short-term temperature and nutrient changes. Limnologica 59, 78-89. http://doi.org/10.1016/j.limno.2016.05.002.

Willén, E., 2000. Phytoplankton in water quality assessment—An indicator concept. In: Heinonen, P., Giuliano, Z., & Van der Beken, A., eds, Hydrological and limnological aspects of lake monitoring. West Sussex, England: Wiley and Sons, Ltd., 57-80. http://doi.org/10.1002/9780470511121.ch6.

Yang, H., Zhao, Y., Wang, J.H., Xiao, W.H., Jarsjö, J., Huang, Y., & Wang, H.J., 2020. Urban closed lakes: nutrient sources, assimilative capacity and pollutant reduction under different precipitation frequencies. Sci. Total Environ. 700, 134531. PMid:31655453. http://doi.org/10.1016/j.scitotenv.2019.134531.

Zahra, Z., Choo, D.H., Lee, H., & Parveen, A., 2020. Cyanobacteria: review of current potentials and applications. Environments 7(2), 13. http://doi.org/10.3390/environments7020013.

Zeileis, A., Cribari-Neto, F., Gruen, B., Kosmidis, I., Simas, A.B., Rocha, A.V., & Zeileis, M.A., 2016. Package ‘betareg’. R package, v.3.1-2 [online]. Retrieved in 2023, August 21, from https://cran.rproject.org/web/packages/betareg/betareg.pdf..

Zhang, Y., Li, M., Dong, J., Yang, H., Van Zwieten, L., Lu, H., & Wang, H., 2021. A critical review of methods for analyzing freshwater eutrophication. Water 13(2), 225. http://doi.org/10.3390/w13020225.

Zhou, B., Cai, X., Wang, S., & Yang, X., 2020. Analysis of the causes of cyanobacteria bloom: a review. J. Resour. Ecol. 11(4), 405-413. http://doi.org/10.5814/j.issn.1674-764x.2020.04.009.

Zohary, T., Padisák, J., & Naselli-Flores, L., 2010. Phytoplankton in the physical environment: beyond nutrients, at the end, there is some light. Hydrobiologia 639(1), 261-269. http://doi.org/10.1007/s10750-009-0032-2.
 


Submitted date:
08/21/2023

Accepted date:
05/15/2024

Publication date:
08/22/2024

66c74c58a9539510477a7fa5 alb Articles
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Acta Limnol. Bras. (Online)

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