Acta Limnologica Brasiliensia
http://www.alb.periodikos.com.br/article/doi/10.1590/S2179-975X7724
Acta Limnologica Brasiliensia
Original Article

Spatial and temporal factors determining the structure of ciliate protist communities in neotropical streams

Fatores espaciais e temporais que determinam a estrutura das comunidades de protistas ciliados em riachos neotropicais

Carolina Leite Guimarães Durán; Felipe Rafael de Oliveira; Matheus Henrique de Oliveira de Matos; Leonardo Antunes Pessoa; Melissa Progênio; Loiani Oliveira Santana; Aline Aparecida Aguiar Ferreira; Luiz Felipe Machado Velho

Downloads: 0
Views: 33

Abstract

Aim: In this study, we focused on patterns of ciliate protist community composition in urban and rural streams.

Methods: We analyzed 12 urban and rural streams during two different periods of the year (rainy and dry seasons) across three different stream mesohabitats (riffles, runs, and pools). We predicted that the species composition of ciliates would differ between types of environments (rural and urban), between basins (Pirapó and Ivaí), between mesohabitats (riffles, runs, and pools), and between seasonal periods. We also expected that ciliate species composition would be similar between streams within the same basin.

Results: Contrary to our expectations, our results showed that the richness and abundance of ciliates were higher in urban streams than in rural streams. In the analysis of beta diversity, we observed that this measure was higher in rural environments, but only during one period (dry season). Among the mesohabitats, no significant alterations in ciliate species composition were noted, contrary to our predictions.

Conclusions: The results obtained in this study demonstrated the effect of multiple spatial (basin, type of environment) and temporal (rainy and dry seasons) factors on the structure of ciliate protists in the water column of neotropical streams. No differences in ciliate attributes were found among the mesohabitats analyzed in this study.

Keywords

streams; urbanization; agriculture; ciliates; mesohabitat

Resumo

Objetivo: O objetivo deste estudo foi investigar os padrões de composição da comunidade de protistas ciliados em riachos urbanos e rurais próximos a um grande centro urbano.

Métodos: Analisamos 12 riachos entre urbanos e rurais durante dois períodos diferentes do ano (estação chuvosa e seca) em três diferentes meso-habitats dos riachos (rápido, remanso e corredeira). Previmos que a composição de espécies de ciliados seria diferente entre os tipos de ambientes (rural e urbano), entre as bacias nos quais os riachos estavam inseridos (Pirapó e Ivaí), entre meso-habitats (rápido, corredeira e remanso) e entre períodos sazonais. Também era esperado que a composição de espécies de ciliados fosse semelhante entre riachos dentro de uma mesma bacia.

Resultados: De forma oposta, os resultados mostraram que a riqueza e abundância de ciliados foram maiores em riachos urbanos do que em riachos rurais. Na análise da diversidade beta, observamos que essa medida foi maior em ambientes rurais, mas apenas durante um período (estação seca). Entre os meso-habitats não foram observadas alterações significativas na composição de espécies de ciliados, contrariando o predito inicialmente.

Conclusões: Os resultados obtidos neste estudo demonstraram o efeito de múltiplos fatores espaciais (bacia, tipo de ambiente) e temporais (estações chuvosas e secas) na estrutura dos protistas ciliados na coluna d'água de riachos neotropicais. Não foram encontradas diferenças nos atributos dos ciliados entre os meso-habitats analisados neste estudo.

Palavras-chave

riachos, urbanização, agricultura, ciliados, mesohabitat

References

Adl, S.M., Bass, D., Lane, C.E., Lukeš, J., Schoch, C.L., Smirnov, A., Agatha, S., Berney, C., Brown, M.W., Burki, F., Cárdenas, P., Čepička, I., Chistyakova, L., del Campo, J., Dunthorn, M., Edvardsen, B., Eglit, Y., Guillou, L., Hampl, V., Heiss, A.A., Hoppenrath, M., James, T.Y., Karnkowska, A., Karpov, S., Kim, E., Kolisko, M., Kudryavtsev, A., Lahr, D.J.G., Lara, E., Le Gall, L., Lynn, D.H., Mann, D.G., Massana, R., Mitchell, E.A.D., Morrow, C., Park, J.S., Pawlowski, J.W., Powell, M.J., Richter, D.J., Rueckert, S., Shadwick, L., Shimano, S., Spiegel, F.W., Torruella, G., Youssef, N., Zlatogursky, V. & Zhang, Q., 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66(1), 4-119. PMid:30257078. http://doi.org/10.1111/jeu.12691.

Alexandre, C.V., Esteves, K.E. & Moura e Mello, M.A.M., 2010. Analysis of fish communities along a rural–urban gradient in a neotropical stream (Piracicaba River Basin, São Paulo, Brazil). Hydrobiol. 641(1), 97-114. http://doi.org/10.1007/s10750-009-0060-y.

Anderson, M.J., Ellingsen, K.E. & McArdle, B.H., 2006. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9(6), 683-693. PMid:16706913. http://doi.org/10.1111/j.1461-0248.2006.00926.x.

Arndt, H., Dietrich, D., Auer, B., Cleven, E.J., Grafenhan, T., Weitere, M. & Mylnikov, A.P., 2000. Functional diversity of heterotrophic flagellates in aquatic ecosystems. Syst. Assoc. 59, 240-268.

Bourdeau, P., & Treshow, M., 1978. Ecosystem response to pollution. In: Butler, G.C., eds. Principles of ecotoxicology (scope 12). Chichester: John Wiley & Sons, 313-330.

Brown, A.V., & Brussock, P.P., 1991. Comparisons of benthic invertebrates between riffles and pools. Hydrobiologia 220(2), 99-108. http://doi.org/10.1007/BF00006542.

Camargo, J.C., 2009. Estrutura e dinâmica da comunidade de protozoários flagelados em riachos tropicais sob influência de atividades humanas [Ph.D. thesis in Ecologia de Ambientes Aquáticos Continentais]. Maringá: Universidade Estadual de Maringá.

Canella, T.F., 2016. Heterogeneidade ambiental explica os padrões de diversidade β taxonômica e funcional em planícies de inundação do Brasil [Ph.D. thesis in Ecologia de Ambientes Aquáticos Continentais]. Maringá: Universidade Estadual de Maringá.

Cunico, A.M., Agostinho, A.A. & Latini, J.D., 2006. Influência da urbanização sobre as assembléias de peixes em três córregos de Maringá, Paraná. Rev. Bras. Zool. 23(4), 1101-1110. http://doi.org/10.1590/S0101-81752006000400018.

Debastiani, C., Meira, B.R., Lansac-Tôha, F.M., Velho, L.F.M. & Lansac-Tôha, F.A., 2016. Protozoa ciliates community structure in urban streams and their environmental use as indicators. Braz. J. Biol. 76(4), 1043-1053. PMid:27191462. http://doi.org/10.1590/1519-6984.08615.

Dias, R.J.P., Souza, P.M., Rossi, M.F., Wieloch, A.H., Silva-Neto, I.D. & D’Agosto, M., 2021. Ciliates as bioindicators of water quality: A case study in the neotropical region and evidence of phylogenetic signals (18S-rDNA). Environ. Pollut. 268(Pt A), 115760. PMid:33162216. http://doi.org/10.1016/j.envpol.2020.115760.

Dias, R.J.P., Wieloch, A.H. & D’Agosto, M., 2008. The influence of environmental characteristics on the distribution of ciliates (Protozoa, Ciliophora) in an urban stream of southeast Brazil. Braz. J. Biol. 68(2), 287-295. PMid:18660956. http://doi.org/10.1590/S1519-69842008000200009.

Fenchel, T., 1987. Ecological physiology: feeding. In: Fenchel, T., ed. Ecology of Protozoa: the biology of free-living phagotrophic protists. Madison: Science Tech Publishers, 32-52.

Foissner, W. & Berger, H., 1996. A user‐friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshw. Biol. 35(2), 375-482. http://doi.org/10.1111/j.1365-2427.1996.tb01775.x.

Gál, B., Szivák, I., Heino, J. & Schmera, D., 2019. The effect of urbanization on freshwater macroinvertebrates–knowledge gaps and future research directions. Ecol. Indic. 104, 357-364. http://doi.org/10.1016/j.ecolind.2019.05.012.

Geisen, S., Mitchell, E.A.D., Wilkinson, D.M., Adl, S., Bonkowski, M., Brown, M.W., Fiore-Donno, A.M., Heger, T.J., Jassey, V.E.J., Krashevska, V., Lahr, D.J.G., Marcisz, K., Mulot, M., Payne, R., Singer, D., Anderson, O.R., Charman, D.J., Ekelund, F., Griffiths, B.S., Rønn, R., Smirnov, A., Bass, D., Belbahri, L., Berney, C., Blandenier, Q., Chatzinotas, A., Clarholm, M., Dunthorn, M., Feest, A., Fernández, L.D., Foissner, W., Fournier, B., Gentekaki, E., Hájek, M., Helder, J., Jousset, A., Koller, R., Kumar, S., La Terza, A., Lamentowicz, M., Mazei, Y., Santos, S.S., Seppey, C.V.W., Spiegel, F.W., Walochnik, J., Winding, A. & Lara, E., 2017. Soil protistology rebooted: 30 fundamental questions to start with. Soil Biol. Biochem. 111, 94-103. http://doi.org/10.1016/j.soilbio.2017.04.001.

Guimarães Durán, C.L., Lansac-Tôha, F.M., Meira, B.R., Santana, L.O., Oliveira, F.R., Matos, M.H.O. & Velho, L.F.M., 2024. Upstream cascade reservoirs drive temporal beta diversity increases through species loss in a dammed river. FEMS Microbiol. Ecol. 100(1), 1-10. PMid:38192043. http://doi.org/10.1093/femsec/fiad165.

Helfman, G.S., Collette, B.B., Facey, D.E. & Bowen, B.W., 2009. The diversity of fishes: biology, evolution, and ecology. Hoboken: John Wiley & Sons.

Horvath, T.G. & Lamberti, G.A., 1999. Mortality of zebra mussel, Dreissena polymorpha, veligers during downstream transport. Freshw. Biol. 42(1), 69-76. http://doi.org/10.1046/j.1365-2427.1999.00462.x.

Huang, J., Huang, L., Wu, Z., Mo, Y., Zou, Q., Wu, N. & Chen, Z., 2019. Correlation of fish assemblages with habitat and environmental variables in a headwater stream section of Lijiang River, China. Sustainability 11(4), 1135. http://doi.org/10.3390/su11041135.

Jeffries, M. & Mills, D., 1990. Freshwater ecology: principles and applications. London: Belhaven Press.

Katayama, F.S., Nunes, L.S.C. & Camargo, A.F.M., 2024. Streams pollution in a luxury tourism municipality in the Serra da Mantiqueira (Southeast Brazil). Acta Limnol. Bras. 36, e16. http://doi.org/10.1590/s2179-975x9523.

Kühl, A.M. & Rocha, C.L.M.S.C., 2010. Rural and urban streams: anthropogenic influences and impacts on water and sediment quality. Int. Rev. Hydrobiol. 95(3), 260-272. http://doi.org/10.1002/iroh.200911190.

Kulaš, A., Gulin, V., Matoničkin Kepčija, R., Žutinić, P., Sertić Perić, M., Orlić, S., Kajan, K., Stoeck, T., Lentendu, G., Čanjevac, I., Martinić, I. & Gligora Udovič, M., 2021. Ciliates (Alveolata, Ciliophora) as bioindicators of environmental pressure: A karstic river case. Ecol. Indic. 124, 107430. http://doi.org/10.1016/j.ecolind.2021.107430.

Lippert, M.A.M., Lansac-Tôha, F.M., Meira, B.R., Velho, L.F.M. & Lansac-Toha, F.A., 2019. Structure and dynamics of the protoplankton community in an environmentally protected urban stream. Braz. J. Biol. 80(4), 844-859. PMid:31800767. http://doi.org/10.1590/1519-6984.222607.

Luo, K., Hu, X., He, Q., Wu, Z., Cheng, H., Hu, Z. & Mazumder, A., 2018. Impacts of rapid urbanization on the water quality and macroinvertebrate communities of streams: a case study in Liangjiang New Area, China. Sci. Total Environ. 621, 1601-1614. PMid:29054671. http://doi.org/10.1016/j.scitotenv.2017.10.068.

Madoni, P. & Bassanini, N., 1999. Longitudinal changes in the ciliated protozoa communities along a fluvial system polluted by organic matter. Eur. J. Protistol. 35(4), 391-402. http://doi.org/10.1016/S0932-4739(99)80048-0.

Madoni, P. & Braghiroli, S., 2007. Changes in the ciliate assemblage along a fluvial system related to physical, chemical and geomorphological characteristics. Eur. J. Protistol. 43(2), 67-75. PMid:17222541. http://doi.org/10.1016/j.ejop.2006.09.004.

Madoni, P., 1984. Estimation of the size of freshwater ciliate populations by a sub-sampling technique. Hydrobiologia 111(3), 201-206. http://doi.org/10.1007/BF00007200.

Madoni, P., 2005. Ciliated protozoan communities and saprobic evaluation of water quality in the hilly zone of some tributaries of the Po River (northern Italy). Hydrobiol. 541(1), 55-69. http://doi.org/10.1007/s10750-004-4667-8.

Mapurunga, M.E.R., Pessoa, Y.V.B., Maria, A.H., Oliveira, J.S. & Terra, B.F., 2024. A influência de filtros ambientais locais na ictiofauna de riachos intermitentes. RCGS 26(2), 134-145. http://doi.org/10.35701/rcgs.v26.1027.

Meira, B.R., Progênio, M., Leite, E.C., Lansac-Tôha, F.M., Durán, C.L.G., Jati, S., Rodrigues, L.C., Lansac-Tôha, F.A., & Velho, L.M.F., 2021. Functional feeding groups of Protist Ciliates (Protist: Ciliophora) on a neotropical flood plain. Ann Limnol Int. J. Limnol. 57, 13. http://doi.org/10.1051/limn/2021009.

Moi, D.A. & Teixeira-de-Mello, F., 2022. Cascading impacts of urbanization on multitrophic richness and biomass stock in neotropical streams. Sci. Total Environ. 806(Pt 4), 151398. PMid:34742800. http://doi.org/10.1016/j.scitotenv.2021.151398.

Munn, M.D., Black, R.W. & Gruber, S.J., 2002. Response of benthic algae to environmental gradients in an agriculturally dominated landscape. J. N. Am. Benthol. Soc. 21(2), 221-237. http://doi.org/10.2307/1468411.

Oliveira, F.R., Lansac-Tôha, F.M., Meira, B.R., Progênio, M. & Velho, L.F.M., 2024. Influence of ecological multiparameters on facets of β-Diversity of freshwater Plankton Ciliates. Microb. Ecol. 87(1), 10. PMid:38057381. http://doi.org/10.1007/s00248-023-02312-9.

Ortega, J.C.G., Bacani, I., Dorado-Rodrigues, T.F., Strüssmann, C., Fernandes, I.M., Morales, J., Mateus, L., Silva, H.P. & Penha, J., 2021. Effects of urbanization and environmental heterogeneity on fish assemblages in small streams. Neotrop. Ichthyol. 19(3), e210050. http://doi.org/10.1590/1982-0224-2021-0050.

Paiva, T.S. & Silva-Neto, I.D., 2004. Ciliate protists from Cabiúnas lagoon (restinga de Jurubatiba, Macaé, Rio de Janeiro) with emphasis on water quality indicator species and description of Oxytricha marcili sp. n. Braz. J. Biol. 64(3A), 465-478. PMid:15622844. http://doi.org/10.1590/S1519-69842004000300010.

Paredes del Puerto, J.M., Paracampo, A.H., García, I.D., Maiztegui, T., Garcia de Souza, J.R., Maroñas, M.E. & Colautti, D.C., 2021. Fish assemblages and water quality in pampean streams (Argentina) along an urbanization gradient. Hydrobiol. 848(19), 4493-4510. http://doi.org/10.1007/s10750-021-04657-z.

Payne, R.J., 2013. Seven reasons why protists make useful bioindicators. Acta Protozool. (Online), 52(3). Retrieved in 2024, September 03, from http://www.eko.uj.edu.pl/apdoi:10.4467/16890027AP.13.0011.1108

Peruço, J.D. 2004. Identificação das principais fontes poluidoras de afluentes da bacia do alto rio Pirapó [Doctoral dissertation in Engenharia Química]. Maringá: Universidade Estadual de Maringá.

Pessoa, L.A., Baumgartner, M.T., Santana Junior, M.P., Pagotto, J.P.A., Pessoa, L.G.A. & Goulart, E., 2021. Effect of land-use types on the ecomorphological structure of fish assemblage in distinct mesohabitats of neotropical streams. Biota Neotrop. 21(3), e20201034. https://doi.org/10.1590/1676-0611-BN-2020-1034.

Primc-Habdija, B., 1988. Trophic relationships of ciliated Protozoa developed under different saprobic conditions in the periphyton of the Sava River. Period. Biol. 90(3), 349-353.

Primc-Habdija, B., Habdija, I. & Radanović, I., 1998. Seasonal changes in trophic structure of periphytic ciliates in relation to discharge regime. Internationale Vereinigung für theoretische und angewandte Limnologie. Verhandlungen 26(3), 1116-1119. https://doi.org/10.1080/03680770.1995.11900893.

R Core Team 2013. R: a language and environment for statistical computing [online]. Retrieved in 2025, May 29, from http://www.R‑project.org/

Risse‐Buhl, U., Schlief, J. & Mutz, M., 2015. Phagotrophic protists are a key component of microbial communities processing leaf litter under contrasting oxic conditions. Freshw. Biol. 60(11), 2310-2322. http://doi.org/10.1111/fwb.12657.

Santos, G.F.D., Garcez, J.R., Freire, G.M., Santos, M., Frisso, R.M., Rodriguez, E.S., Cavalcante, L.K.F., Olimpio, R.G., Marinho, A.F.C., Amaral Junior, W.P., Brito, V.G.M. & Cavalcante, J.L.C., 2024. O efeito de defensivos agrícolas sobre a reprodução de peixes nativos. Rev. Foco 17(4), e4853. http://doi.org/10.54751/revistafoco.v17n4-056.

Savić, A., Zawal, A., Stępień, E., Pešić, V., Stryjecki, R., Pietrzak, L., Filip, E., Skorupski, J. & Szlauer-Łukaszewska, A., 2022. Main macroinvertebrate community drivers and niche properties for characteristic species in urban/rural and lotic/lentic systems. Aquat. Sci. 84(1), 1-14. http://doi.org/10.1007/s00027-021-00832-5.

Scoarize, M.M.R., Pinha, G.D., Pazianoto, L.H.R. & Benedito, E., 2024. Stream environmental conditions are homogenised outside a protected area, but fungal beta diversity remains unchanged. Mycol. Prog. 23(1), 12. http://doi.org/10.1007/s11557-024-01952-6.

Segovia, B.T., Lansac-Toha, F.M., Meira, B.R., Cabral, A.F., Lansac-Tôha, F.A. & Velho, L.F.M., 2016. Anthropogenic disturbances influencing ciliate functional feeding groups in impacted tropical streams. Environ. Sci. Pollut. Res. Int. 23(19), 20003-20016. PMid:27439753. http://doi.org/10.1007/s11356-016-7185-0.

Sieber, G., Beisser, D., Bock, C. & Boenigk, J., 2020. Protistan and fungal diversity in soils and freshwater lakes are substantially different. Sci. Rep. 10(1), 20025. PMid:33208814. http://doi.org/10.1038/s41598-020-77045-7.

Souza, F. & Klepka, V., 2012. A importância da hidrografia sobre a biogeografia aquática regional: um caso dos afluentes da bacia do Rio Paraná. Rev. Meio Amb. Sustentab. 2(1), 68-90. https://doi.org/10.22292/mas.v2i1.123.

Townsend, A.M., 1980. Response of selectedtree species to sodium chloride. J. Am. Soc. Hortic. Sci. 105(6), 878-883. http://doi.org/10.21273/JASHS.105.6.878.

Vargas, C., Audic, S., Henry, N., Decelle, J., Mahé, F., Logares, R., Lara, E., Berney, C., Le Bescot, N., Probert, I., Carmichael, M., Poulain, J., Romac, S., Colin, S., Aury, J.-M., Bittner, L., Chaffron, S., Dunthorn, M., Engelen, S., Flegontova, O., Guidi, L., Horák, A., Jaillon, O., Lima-Mendez, G., Lukeš, J., Malviya, S., Morard, R., Mulot, M., Scalco, E., Siano, R., Vincent, F., Zingone, A., Dimier, C., Picheral, M., Searson, S., Kandels-Lewis, S., Acinas, S.G., Bork, P., Bowler, C., Gorsky, G., Grimsley, N., Hingamp, P., Iudicone, D., Not, F., Ogata, H., Pesant, S., Raes, J., Sieracki, M.E., Speich, S., Stemmann, L., Sunagawa, S., Weissenbach, J., Wincker, P., Karsenti, E., Boss, E., Follows, M., Karp-Boss, L., Krzic, U., Reynaud, E.G., Sardet, C., Sullivan, M.B. & Velayoudon, D., 2015. Eukaryotic plankton diversity in the sunlit ocean. Science 348(6237), 1261605. PMid:25999516. http://doi.org/10.1126/science.1261605.

Velho, L.F.M., Castro, S.D.F.R., Lansac-Tôha, F.M., Meira, B.R., Oliveira, F.R., Alves, G.M. & Lansac-Tôha, F.A., 2021. Spatial and temporal variation in species composition of ciliates communities (Alveolata, Ciliophora) from tropical urban and rural streams. Int. J. Limnol. 57, 24. http://doi.org/10.1051/limn/2021022.

Walsh, C.J., Roy, A.H., Feminella, J.W., Cottingham, P.D., Groffman, P.M. & Morgan 2nd, R.P., 2005. The urban stream syndrome: current knowledge and the search for a cure. J. N. Am. Benthol. Soc. 24(3), 706-723. http://doi.org/10.1899/04-028.1.

Walsh, C.J., Sharpe, A.K., Breen, P.F. & Sonneman, J.A., 2001. Effects of urbanization on streams of the Melbourne region, Victoria, Australia. I. Benthic macroinvertebrate communities. Freshw. Biol. 46(4), 535-551. http://doi.org/10.1046/j.1365-2427.2001.00690.x.

Wang, C., Xu, M., Xuan, J., Li, H., Zheng, S., Zhao, Y., Zhang, W. & Xiao, T., 2021. Impact of the warm eddy on planktonic ciliate, with an emphasis on tintinnids as bioindicator species. Ecol. Indic. 133, 108441. http://doi.org/10.1016/j.ecolind.2021.108441.

Wang, J., Soininen, J., Zhang, Y., Wang, B., Yang, X. & Shen, J., 2012. Patterns of elevational beta diversity in microand macroorganisms. Glob. Ecol. Biogeogr. 21(7), 743-750. http://doi.org/10.1111/j.1466-8238.2011.00718.x.

Wang, L. & Kanehl, P., 2003. Influences of watershed urbanization and instream habitat on macroinvertebrates in cold water streams. J. Am. Water Resour. Assoc. 39(5), 1181-1196. http://doi.org/10.1111/j.1752-1688.2003.tb03701.x.

Wang, L., Lyons, J., Kanehi, P., Bannerman, R. & Emmons, E., 2000. Watershed urbanization and changes in fish communities in southeastern Wisconsin streams. J. Am. Water Resour. Assoc. 36(5), 1173-1189. http://doi.org/10.1111/j.1752-1688.2000.tb05719.x.

Weaver, L.A. & Garman, G.C., 1994. Urbanization of a watershed and historical changes in a stream fish assemblage. Trans. Am. Fish. Soc. 123(2), 162-172. http://doi.org/10.1577/1548-8659(1994)123<0162:UOAWAH>2.3.CO;2.

Weisse, T. & Sonntag, B., 2016. Ciliates in planktonic food webs: communication and adaptive response. In: Witzany, G. & Nowacki, M., eds. Biocommunication of ciliates. Cham: Springer, 351-372. http://doi.org/10.1007/978-3-319-32211-7_19.

Weisse, T., 1991. The annual cycle of heterotrophic freshwater nanoflagellates: role of bottom‑up versus top‑down control. J. Plankton Res. 13(1), 167-185. http://doi.org/10.1093/plankt/13.1.167.

Whittaker, R.H., 1972. Evolution and measurement of species diversity. Taxon 21(2-3), 213-251. http://doi.org/10.2307/1218190.

Wolff, L.L. & Hahn, S.N., 2017. Fish habitat associations along a longitudinal gradient in a preserved coastal Atlantic stream, Brazil. Zool. 34, 1-13. https://doi.org/10.3897/zoologia.34.e12975.

Zingel, P., 2005. Vertical and seasonal dynamics of planktonic ciliates in a strongly stratified hypertrophic lake. Hydrobiol. 547(1), 163-174. http://doi.org/10.1007/s10750-005-4157-7.
 


Submitted date:
09/03/2024

Accepted date:
05/29/2025

Publication date:
07/23/2025

68812ba8a953955a5960cd83 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections