Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X4224
Acta Limnologica Brasiliensia
Thematic Section: Neotropical Zooplankton Symposium

Microcrustaceans structure determined by the type and trophic state of lakes

Estrutura de microcrustáceos determinada pelo tipo e estado trófico dos lagos

Bharguan Pizzol Nogueira; Camila Moreira-Silva; Thaís Coimbra Marigo; Gilmar Perbiche-Neves

http://dx.doi.org/10.1590/S2179-975X4224 Acta Limnol. Bras. (Online), vol.37, e102, 2025
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Abstract

Aim: In this study, we investigated the response of microcrustaceans composition, diversity and abundance (Cladocera and Copepoda) to the lake’s origin (natural and man-made) and trophic state (mesotrophic and eutrophic, with natural eutrophication and artificial eutrophication). We tested the following hypotheses: (I) the increase in the abundance of certain microcrustacean species may indicate a rise in the trophic level; (II) the richness and abundance vary amongst lakes and are higher in the lake with natural eutrophication; and (III) the microcrustaceans abundance is associate with high primary productivity, being higher in the eutrophic environment with artificial eutrophication.

Methods: The study was conducted in a segment of the Paranapanema River basin, in southeastern Brazil, focusing on five lakes spanning an eight-kilometer stretch, to understand the different organisms' responses to distinct conditions of aquatic environments. Sampling was carried out bimonthly over the course of a year.

Results: A principal component analysis (PCA) separated three types of lakes: eutrophic (natural and man-made) to mesotrophic. Additionally, 25 taxa were found. SIMPER analysis filtered six species with more than 70% dissimilarity contribution. Five species exhibited differences amongst the lakes, one species correlated with natural variables as depth. The redundancy analysis associated the Bosminopsis deitersi abundance with man-made eutrophic lakes and with the variables electrical conductivity, phosphorus, nitrogen, chlorophyll-a, and hardness. High abundances of B. deitersi indicated artificial eutrophication especially in man-made lakes, while natural lakes with natural eutrophication were not favorable environments for the increase of B. deitersi abundance.

Conclusions: This study highlights the neotropical oxbow lakes, emphasizing the significance of physicochemical characterization, detailed temporal sampling, and lake classification by origin and trophic level.

Keywords

anthropic impacts; oxbow lakes; Neotropical region; zooplankton

Resumo

Objetivo: Neste estudo, nós investigamos a resposta da composição, diversidade e abundância de microcrustáceos (Cladocera e Copepoda) à origem do lago (natural e artificial) e ao estado trófico (mesotrófico e eutrófico, com eutrofização natural e eutrofização artificial). Testamos as seguintes hipóteses: (I) o aumento na abundância de certas espécies de microcrustáceos pode indicar um aumento no nível trófico; (II) a riqueza e a abundância variam entre os lagos e são maiores no lago com eutrofização natural; e (III) a abundância de microcrustáceos está associada à alta produtividade primária, sendo maior no ambiente eutrófico com eutrofização artificial.

Métodos: O estudo foi realizado em um segmento da bacia do rio Paranapanema, no sudeste do Brasil, com foco em cinco lagos em um trecho de oito quilômetros, para entender as respostas dos diferentes organismos em condições distintas de ambientes aquáticos. A amostragem foi realizada bimestralmente ao longo de um ano.

Resultados: Uma análise de componentes principais (PCA) separou três tipos de lagos: eutróficos (naturais e artificiais) a mesotróficos. Adicionalmente, 25 táxons foram encontrados. A análise SIMPER filtrou seis espécies com mais de 70% de contribuição de dissimilaridade. Cinco espécies apresentaram diferenças entre os lagos, uma espécie correlacionada com variáveis naturais, como profundidade. A análise de redundância associou a abundância de Bosminopsis deitersi com lagos eutróficos artificiais e com as variáveis condutividade elétrica, fósforo, nitrogênio, clorofila-a e dureza. Altas abundâncias de B. deitersi indicaram eutrofização artificial especialmente em lagos artificiais, enquanto lagos naturais com eutrofização natural não foram ambientes favoráveis para o aumento da abundância de B. deitersi.

Conclusões: Este estudo destaca os lagos de meandros neotropicais, enfatizando a importância da caracterização físico-química, da amostragem temporal detalhada e da classificação dos lagos por origem e nível trófico.

Palavras-chave

impactos antrópicos; lagos de meandros; região Neotropical; zooplâncton

References

Barnett, A., & Beisner, B.E., 2007. Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology 88(7), 1675-1686. PMid:17645014. http://doi.org/10.1890/06-1056.1.

Bonecker, C.C., Nagae, M.Y., Bletller, M.C.M., Velho, L.F.M., & Lansac-Tôha, F.A., 2007. Zooplankton biomass in tropical reservoirs in southern Brazil. Hydrobiologia 579(1), 115-123. http://doi.org/10.1007/s10750-006-0391-x.

Bouvy, M., Pagano, M., & Troussellier, M., 2001. Effects of a cyanobacterial bloom (Cylindrospermopsis raciborskii) on bacteria and zooplankton communities in Ingazeira reservoir (northeast Brazil). Aquat. Microb. Ecol. 25(3), 215-227. http://doi.org/10.3354/ame025215.

Branco, C.W.C., Rocha, M.-I.A., Pinto, G.F.S., Gômara, G.A., & Filippo, R.D., 2002. Limnological features of Funil Reservoir (R.J., Brazil) and indicator properties of rotifers and cladocerans of the zooplankton community. Lakes Reserv. 7(2), 87-92. http://doi.org/10.1046/j.1440-169X.2002.00177.x.

Brito, S.L., Maia-Barbosa, P.M., & Pinto-Coelho, R.M., 2013. Length-weight relationships and biomass of the main microcrustacean species of two large tropical reservoirs in Brazil. Braz. J. Biol. 73(3), 593-604. PMid:24212700. http://doi.org/10.1590/S1519-69842013000300017.

Brucet, S., Boix, D., Gascón, S., Sala, J., Quintana, X.D., Badosa, A., Søndergaard, M., Lauridsen, T.L., & Jeppesen, E., 2009. Species richness of crustacean zooplankton and trophic structure of brackish lagoons in contrasting climate zones: north temperate Denmark and Mediterranean Catalonia (Spain). Ecography 32(4), 692-702. http://doi.org/10.1111/j.1600-0587.2009.05823.x.

Choi, J.Y., Jeong, K.S., Kim, S.K., La, G.H., Chang, K.H., & Joo, G.J., 2014. Role of macrophytes as microhabitats for zooplankton community in lentic freshwater ecosystems of South Korea. Ecol. Inform. 24, 177-185. http://doi.org/10.1016/j.ecoinf.2014.09.002.

Companhia de Tecnologia Ambiental do Estado de São Paulo – CETESB, 2014. Indicadores de qualidade das águas [online]. Retrieved in 2023, July 1, from http://www.cetesb.sp.gov.br/.

Dantas-Silva, L.T., & Dantas, E.W., 2013. Zooplankton (Rotifera, Cladocera and Copepoda) and the eutrophication in reservoirs from northeastern Brazil. Oecol. Aust. 17(2), 243-248. http://dx.doi.org/10.4257/oeco.2013.1702.06.

Debastiani-Júnior, J.R., Elmoor-Loureiro, L.M.A., & Nogueira, M.G., 2015. High taxonomic resolution as a determinant on finding new species and new records in the Río de La Plata basin: a case on Chydoridae (Crustacea: Branchiopoda: Cladocera). Nauplius 23(1), 21-30. http://doi.org/10.1590/S0104-64972015002301.

Debastiani-Júnior, J.R., Elmoor-Loureiro, L.M.A., & Nogueira, M.G., 2016. Habitat architecture influencing microcrustaceans composition: a case study on freshwater Cladocera (Crustacea Branchiopoda). Braz. J. Biol. 76(1), 93-100. PMid:26909628. http://doi.org/10.1590/1519-6984.13514.

Dubey, D., & Dutta, V., 2020. Nutrient Enrichment in lake ecosystem and its effects on algae and Macrophytes. In: Shukla, V., Kumar, N., eds. Environmental concerns and sustainable development. Singapore: Springer Nature Singapore, 81-126. http://doi.org/10.1007/978-981-13-6358-0_5.

Ejsmont-Karabin, J., & Karabin, A., 2013. The suitability of zooplankton as lake ecosystem indicators: crustacean trophic state index. Pol. J. Ecol. 61(3), 561-573.

Elmoor-Loureiro, L.M.A. 1997. Manual de identificação de cladóceros límnicos do Brasil. Brasília: Universa.

Garcia, X.F., Schnauder, I., & Pusch, M.T., 2012. Complex hydromorphology of meanders can support benthic invertebrate diversity in rivers. Hydrobiologia. 685, 49-68. http://doi-org/10.1007/s10750-011-0905-z.

Ger, K., Hansson, L.-A., & Lürling, M., 2014. Understanding cyanobacteria-zooplankton interactions in a more eutrophic world. Freshw. Biol. 59(9), 1783-1798. http://doi.org/10.1111/fwb.12393.

Ghidini, A.R., Serafim-Júnior, M., Perbiche-Neves, G., & Brito, L.D., 2009. Distribution of planktonic cladocerans (Crustacea: Branchiopoda) of a shallow eutrophic reservoir (Paraná State, Brazil). Pan-Am. J. Aquat. Sci. 4(3), 294-305.

Goltermann, H.L., Clymos, R.S., & Ohnstad, M.A.M., 1978. Methods for physical and chemical analysis of fresh water. Oxford: Blackwell Scientific Publication.

Goswami, S.C., 2004. Zooplankton methodology, collection & identification: a field manual. Dona Paula, Goa: National Institute of Oceanography.

Guevara, G., Lozano, P., Reinoso, G., & Villa, F., 2009. Horizontal and seasonal patterns of tropical zooplankton from the eutrophic Prado Reservoir (Colombia). Limnologica Online 39(2), 128-139. http://doi.org/10.1016/j.limno.2008.03.001.

Güntzel, A., Panarelli, E., Silva, W., & Roche, K., 2010. Influence of connectivity on Cladocera diversity in oxbow lakes in the Taquari River floodplain (MS, Brazil). Acta Limnol. Bras. 22(1), 93-101. http://doi.org/10.4322/actalb.02201012.

Hammer, O., Harper, D.A.T., & Ryan, P.D., 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electronica (Online). 4(1), 1-9. Retrieved in 2023, July 1, from http://palaeo-electronica.org/2001_1/past/issue1_01.htm.

Hébert, M.-P., Fugère, V., Beisner, B.E., Barbosa Da Costa, N., Barrett, R.D.H., Bell, G., Shapiro, B.J., Yargeau, V., Gonzalez, A. & Fussmann, G.F., 2021. Widespread agrochemicals differentially affect zooplankton biomass and community structure. Ecol. Appl., 31(7), e02423. http://doi.org/10.1002/eap.2423.

Illyová, M., & Pastuchová, Z., 2012. The zooplankton communities of small water reservoirs with different trophic conditions in two catchments in western Slovakia. Limnologica 42(4), 271-281. http://doi.org/10.1016/j.limno.2012.08.004.

Karpowicz, M., Zieliński, P., Grabowska, M., Ejsmont-Karabin, J., Kozłowska, J., & Feniova, I., 2020. Effect of eutrophication and humification on nutrient cycles and transfer efficiency of matter in freshwater food webs. Hydrobiologia 847(11), 2521-2540. http://doi.org/10.1007/s10750-020-04271-5.

Keppeler, E.C., & Hardy, E.R., 2004. Abundance and composition of Rotifera in an abandoned meander lake (Lago Amapá) in Rio Branco, Acre, Brazil. Rev. Bras. Zool. 21(2), 233-241. http://doi.org/10.1590/S0101-81752004000200011.

Lamparelli, M.C., 2004. Grau de trofia em corpos d’água do Estado de São Paulo: avaliação dos métodos de monitoramento [Tese de Doutorado em Ciências]. São Paulo: Instituto de Biociências, Universidade de São Paulo.

Landa, G.G., Barbosa, F.A.R., Rietzler, A.C., & Maia-Barbosa, P.M., 2007. Thermocyclops decipiens (Kiefer, 1929) (Copepoda, Cyclopoida) as indicator of water quality in the State of Minas Gerais, Brazil. Braz. Arch. Biol. Technol. 50(4), 695-705. http://doi.org/10.1590/S1516-89132007000400015.

Mackereth, F., Heron, J., & Talling, J.F., 1978. Water analysis: some revised methods for limnologist. London: Freshwater Biological Association.

Matsumura-Tundisi, T., & Tundisi, J.G., 2003. Calanoida (Copepoda) species composition changes in the reservoirs of São Paulo State (Brazil) in the last twenty years. Hydrobiologia 504(1), 215-222. http://doi.org/10.1023/B:HYDR.0000008521.43711.35.

Matsumura-Tundisi, T., & Tundisi, J.G., 2005. Plankton richness in a eutrophic reservoir (Barra Bonita Reservoir, SP, Brazil). Hydrobiologia 542(1), 367-378. http://doi.org/10.1007/s10750-004-9461-0.

Moroz-Caccia Gouveia, I.C., 2018. Atlas geoambiental da bacia hidrográfica do Rio Paranapanema. Presidente Prudente: FCT/UNESP.

Muñoz-Colmenares, M.E., Soria, J.M., & Vicente, E., 2021. Can zooplankton species be used as indicators of trophic status and ecological potential of reservoirs? Aquat. Ecol. 55(4), 1143-1156. http://doi.org/10.1007/s10452-021-09897-8.

Napiórkowski, P., & Napiórkowska, T., 2017. Limnophase versus potamophase: how hydrological connectivity affects the zooplankton community in an oxbow lake (Vistula River, Poland). Ann. Limnol. –. Int. J. Lim. 53, 143-151. http://doi.org/10.1051/limn/2017001.

Neves, I.F., Rocha, O., Roche, K.F., & Pinto, A.A., 2003. Zooplankton community structure of two marginal lakes of the River Cuiabá (Mato Grosso, Brazil) with analysis of Rotifera and Cladocera diversity. Braz. J. Biol. 63(2), 329-343. PMid:14509855. http://doi.org/10.1590/S1519-69842003000200018.

Nogueira, M.G., 2001. Zooplankton composition, dominance and abundance as indicators of environmental compartmentalization in Jurumirim Reservoir (Paranapanema River), São Paulo, Brazil. Hydrobiologia 455(1), 1-18. http://doi.org/10.1023/A:1011946708757.

Nogueira, M.G., Oliveira, P.C.R., & Britto, Y.T., 2008. Zooplankton assemblages (Copepoda and Cladocera) in a cascade of reservoirs of a large tropical river (SE Brazil). Limnetica 27(1), 151-170. http://doi.org/10.23818/limn.27.13.

Ochocka, A., & Pasztaleniec, A., 2016. Sensitivity of plankton indices to lake trophic conditions. Environ. Monit. Assess. Online 188(11), 622. PMid:27752916. http://doi.org/10.1007/s10661-016-5634-3.

Oksanen, J.F., Blanchet, G., Friendly, M., Kindt, R., Legendre, P., Mcglinn, D., Minchin, P.R., O’hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., & Wagner, H., 2018. Vegan: Community Ecology Package. R package version 2.56. Vienna: R Development Core Team. Retrieved in 2023, July 1, from https://CRAN.R-project.org/package=vegan.

Paquette, C., Griffiths, K., Gregory-Eaves, I., & Beisner, B.E., 2022. Zooplankton assemblage structure and diversity since pre-industrial times in relation to land use. Glob. Ecol. Biogeogr. 31(11), 2337-2352. http://doi.org/10.1111/geb.13575.

Perbiche-Neves, G., & Nogueira, M.G., 2010. Multi-dimensional effects on Cladoceran (Crustacea, Anomopoda) assemblages in two cascade reservoirs in Southeast Brazil. Lakes Reserv. 15(2), 139-152. http://doi.org/10.1111/j.1440-1770.2010.00429.x.

Perbiche-Neves, G., & Nogueira, M.G., 2013. Reservoir design and operation: effects on aquatic biota—a case study of planktonic copepods. Hydrobiologia 707(1), 187-198. http://doi.org/10.1007/s10750-012-1425-1.

Perbiche-Neves, G., Boxshall, G.A., Previattelli, D., Nogueira, M.G., & Rocha, C.E.F.D., 2015. Identification guide to some Diaptomid species (Crustacea, Copepoda, Calanoida, Diaptomidae) of “de la Plata” River Basin (South America). ZooKeys 497(497), 1-111. PMid:25931959. http://doi.org/10.3897/zookeys.497.8091.

Perbiche-Neves, G., da Rocha, C.E.F., & Nogueira, M.G., 2014. Estimating cyclopoid copepod species richness and geographical distribution (Crustacea) across a large hydrographical basin: comparing between samples from water column (plankton) and macrophyte stands. Zoologia Curitiba 31(3), 239-244. http://doi.org/10.1590/S1984-46702014000300005.

Perbiche-Neves, G., Fileto, C., Laço-Portinho, J., Troguer, A., & Serafim-Júnior, M., 2013. Relations among planktonic rotifers, cyclopoid copepods, and water quality in two Brazilian reservoirs. Lat. Am. J. Aquat. Res. 41(1), 138-149. http://doi.org/10.3856/vol41-issue1-fulltext-11.

Perbiche-Neves, G., Moacyr Junior, M., Ghidini, A., & Brito, L., 2007. Spatial and temporal distribution of Copepoda (Cyclopoida and Calanoida) of an eutrophic reservoir in the basin of upper Iguaçu River, Paraná, Brazil. Acta Limnol. Bras. 19(4), 393-406.

Perbiche-Neves, G., Saito, V.S., Previattelli, D., Rocha, C.E.F., & Nogueira, M.G., 2016. Cyclopoid copepods as bioindicators of eutrophication in reservoirs: do patterns hold for large spatial extents? Ecol. Indic. 70, 340-347. http://doi.org/10.1016/j.ecolind.2016.06.028.

Picapedra, P.H.S., Fernandes, C., Taborda, J., Baumgartner, G. & Sanches, P.V., 2020. A long-term study on zooplankton in two contrasting cascade reservoirs (Iguaçu River, Brazil): effects of inter-annual, seasonal, and environmental factors. PeerJ. 8, e8979. http://doi.org/10.7717/peerj.8979.

Pinto-Coelho, R.M., Bezerra-Neto, J.F., & Morais-Jr, C.A., 2005. Effects of eutrophication on size and biomass of crustacean zooplankton in a tropical reservoir. Braz. J. Biol. 65(2), 325-338. PMid:16097736. http://doi.org/10.1590/S1519-69842005000200017.

Reid, J.W., 1985. Chave de identificação e lista de referências bibliográficas para as espécies continentais sulamericanas de vida livre da ordem Cyclopoida (Crustacea, Copepoda). Bolm. Zool.. 9, 17-143. http://doi.org/10.11606/issn.2526-3358.bolzoo.1985.122293.

Rietzler, A.C., Matsumura-Tundisi, T., & Tundisi, J.G., 2002. Life cycle, feeding and adaptive strategy implications on the co-occurrence of Argyrodiaptomus furcatus and Notodiaptomus iheringi in Lobo-Broa Reservoir (SP, Brazil). Braz. J. Biol. 62(1), 93-105. PMid:12185928. http://doi.org/10.1590/S1519-69842002000100012.

Saito, V.S., Siqueira, T., & Fonseca-Gessner, A., 2015. Should phylogenetic and functional diversity metrics compose macroinvertebrate multimetric indices for stream biomonitoring? Hydrobiologia 745(1), 167-179. http://doi.org/10.1007/s10750-014-2102-3.

Sendacz, S., Caleffi, S., & Santos-Soares, J., 2006. Zooplankton biomass of reservoirs in different trophic conditions in the State of São Paulo, Brazil. Braz. J. Biol. 66(1B), 337-350. PMid:16710526. http://doi.org/10.1590/S1519-69842006000200016.

Silva, C.O.R., Junior, A., Perbiche-Neves, G., Pinheiro, A.P., & Lacerda, S.R., 2020. Baixa riqueza zooplanctônica indicando condições adversas de seca e eutrofização em um reservatório no Nordeste do Brasil. Iheringia, Sér. Zool. Online 110, e2020009. http://doi.org/10.1590/1678-4766e2020009.

Silva, W.M., 2011. Potential use of Cyclopoida (Crustacea, Copepoda) as trophic state indicators in tropical reservoirs. Oecol. Aust. 15(3), 511-521. http://doi.org/10.4257/oeco.2011.1503.06.

Ueda, H., & Reid, J.W., 2003. Copepoda: Cyclopoida – genera Mesocyclops and Thermocyclops. In: Dumont, H.J.F., ed. Guides to the identification of the microinvertebrates of the continental waters of the world. Netherlands: Backhuys Publishers, 1-316.

Valderrama, J.C., 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Mar. Chem. 10(2), 109-122. http://doi.org/10.1016/0304-4203(81)90027-X.

Wang, S., Xie, P., & Geng, H., 2010. The relative importance of physicochemical factors and crustacean zooplankton as determinants of rotifer density and species distribution in lakes adjacent to the Yangtze River, China. Limnologica 40(1), 1-7. http://doi.org/10.1016/j.limno.2009.03.001.

Wetzel, R.G., & Likens, G.E., 2000. Limnological analyses. New York: Springer, 3 ed. http://doi.org/10.1007/978-1-4757-3250-4.

Wurtsbaugh, W.A., Paerl, H.W. & Dodds, W.K., 2019. Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum. WIREs Water. 6(5), e1373. http://doi.org/10.1002/wat2.1373.

Zhou, M., Zhou, Z. & Chen, W., 2023. Effects of floods on zooplankton community structure in the huayanghe lake. Diversity. 15(2), 250. http://doi.org/10.3390/d15020250.
 

Submitted date:
04/22/2024

Accepted date:
11/12/2024

Publication date:
02/06/2025

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