Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X6224
Acta Limnologica Brasiliensia
Seção Temática: Simpósio de Zooplâncton Neotropical

Epistylid ciliates as epibionts on calanoid copepods in an Amazonian floodplain lake (Batata Lake)

Ciliados epistilídeos epibiontes em copépodes calanóides em um lago amazônico de planície de inundação (Lago Batata)

Wésley Altino Flores; Pedro Mendes de Souza; Iollanda Ivanov Pereira Josué; Roberto Júnio Pedroso Dias; Reinaldo Luiz Bozelli

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Abstract

Aim: The main objective was to investigate changes in the prevalence and infestation intensity of the epibiotic relationship (ciliates/calanoids) in relation to the impact of bauxite tailings (natural and impacted areas) during two distinct periods of the hydrological pulse (rising and high-water).

Methods: The hydrological pulse of this system can be characterized with four distinct phases: rising, high-water, falling, and low-water. After degradation by bauxite tailings for ten years (1979-1989), and despite an ongoing long-term ecological restoration process, it is still possible to recognize two distinct regions in the lake: the area impacted by the tailings and the natural area. We sampled zooplankton (calanoids and epibiont ciliates) and limnological variables during the high-water period (March 2015) and rising-water period (June 2019) at twelve sampling points in Lake Batata, six in the impacted area and six in the non-impacted area.

Results: This is the first record of peritrichous epibiont ciliates Epistylis sp. colonizing calanoid copepods in Amazonian ecosystems (Lake Batata, Pará, Brazil). We recorded epibiont ciliates in the calanoid copepodite and adult stages, as well as the main location sites on the thorax and abdomen. Our study recorded a significant difference in the prevalence and mean infestation intensity between the natural and bauxite tailings-impacted areas, and in the prevalence of infestation between the rising -water (2015) and high-water (2019) collections. The prevalence of infestation was higher in the impacted area and during the rising-water period.

Conclusions: Although the host/epibiont/environment interaction is complex and requires analysis with a larger number of temporal samples, this study records a clear effect of flooding in this Amazonian system on the spatial and temporal dynamics of epibiont ciliates associated with calanoid copepods.

Keywords

bauxite tailings; epibiosis; Epistylis; flood pulse; Peritrichi

Resumo

Objetivo: O objetivo principal foi investigar mudanças na prevalência e intensidade de infestação da relação epibiótica entre ciliados e calanóides em relação ao impacto por rejeito de bauxita (área natural e impactada) e em dois distintos períodos do pulso hidrológico (rising and high-water).

Métodos: O pulso hidrológico desse sistema pode ser caracterizado por quatro fases distintas: enchente, águas-altas, vazante e águas-baixas. Após longa deposição de rejeitos de bauxita (1979-1989), e apesar de um processo de restauração ecológica de longo prazo em andamento, ainda é possível reconhecer duas regiões distintas no lago: área impactada pelo rejeito e área natural. Nós amostramos o zooplâncton (calanóides e ciliados epibiontes) e as variáveis limnológicas durante os períodos de enchente (março de 2015) e de águas altas (junho de 2019) em doze pontos de coleta no Lago Batata, seis deles na área impactada e seis na área não impactada.

Resultados: Este é o primeiro registro de ciliados epibiontes peritríqueos Epistylis sp. colonizando copépodes calanóides em ecossistemas amazônicos (Lago Batata, Pará, Brasil). Registramos os ciliados epibiontes nas fases de copepodito e adulto, bem como sítio de localização principal no tórax e no abdômen. Nosso estudo registrou significativa diferença entre a prevalência e intensidade média de infestação entre as áreas natural e impactada por rejeito de bauxita, e na prevalência de infestação entre as coletas realizadas na enchente (2015) e águas altas (2019). A prevalência de infestação foi maior na área impactada e no período de enchente.

Conclusões: Embora interação hospedeiro/epibionte/ambiente seja complexa e necessite de uma análise com número maior de amostras temporais, esse estudo registra claro efeito da inundação nesse sistema amazônico sobre a dinâmica espacial e temporal dos ciliados epibiontes associados aos copépodes calanóides.

Palavras-chave

rejeito de bauxita; epibiose; Epistylis; pulso de inundação; Peritrichia

Referências

Anesio, A.M., Abreu, P.C., & de Assis Esteves, F., 1997. Influence of the hydrological cycle on the bacterioplankton of an impacted clear water Amazonian lake. Microb. Ecol. 34(1), 66-73. PMid:9178607. http://doi.org/10.1007/s002489900035.

Bickel, S.L., Tang, K.W., & Grossart, H.P., 2012. Ciliate epibionts associated with crustacean zooplankton in German lakes: distribution, motility and bacterivory. Front. Microbiol. 3, 243-248. PMid:22783247. http://doi.org/10.3389/fmicb.2012.00243.

Burris, Z.P., & Dam, H.G., 2014. Deleterious effects of the ciliate epibiont Zoothamnium sp. on fitness of the copepod Acartia tonsa. J. Plankton Res. 36(3), 788-799. http://doi.org/10.1093/plankt/fbt137.

Cabral, A.F., Dias, R.J.P., Oliveira, V.C., Alves, R.G., & D’Agosto, M., 2018. Rhabdostylid Ciliates (Ciliophora, Peritrichia, Epistylididae) as Epibionts on Chironomid Larvae: Evidence of High Specificity and Association with Organic Pollution. Zoolog. Sci. 35(6), 514-520. PMid:30520356. http://doi.org/10.2108/zs180026.

Cabral, A.F., Dias, R.J.P., Utz, L.R., Alves, R.G., & D’Agosto, M., 2010. Spatial and temporal occurrence of Rhabdostyla cf. chironomi Kahl, 1933 (Ciliophora, Peritrichia) as an epibiont on chironomid larvae in a lotic system in the neotropics. Hydrobiologia 644(1), 351-359. http://doi.org/10.1007/s10750-010-0202-2.

Cabral, A.F., Utz, L.R.P., & Velho, L.F.M., 2017. Structure and distribution of ciliate epibiont communities in a tropical floodplain. Hydrobiologia 787(1), 167-180. http://doi.org/10.1007/s10750-016-2955-8.

Cardoso, S.J., Bozelli, R.L., Roland, F., Esteves, F.D.A., Barros, M.P.F., Caramaschi, É.P., Leal, J.J.F., Resende, N.S., Ribeiro, E.G., Scarano, F.R., & Huszar, V.L.M., 2023. From virus to igapó forest: a systematic review of 35 years monitoring of an Amazonian Lake impacted by bauxite tailings (Batata Lake). Acta Limnol. Bras. Online 35, e2. http://doi.org/10.1590/s2179-975x5922.

Cook, J.A., Chubb, J.C., & Veltkamp, 1998. Epibionts of Asellus aquaticus (L.)(Crustacea, Isopoda): an SEM study. Freshw. Biol. 39(3), 423-438. http://doi.org/10.1046/j.1365-2427.1998.00286.x.

Corre, P.S., Abadilla, M.R.C.S., Arnaldo, M.N.L., Irlanda, M.T.S., Mariano, A.C.P., Dogma Junior, I.J., & Papa, R.D.S., 2020. Vorticella and Colacium as epibionts of copepods in Pasig river, Philippines. Philipp. J. Syst. Biol. 14(1), 1-8. https://doi.org/10.26757/pjsb2020a14008.

Dias, R.J.P., Cabral, A.F., Martins, R.T., Stephan, N.N.C., Silva‐Neto, I.D.D., Alves, R.D.G., & D’Agosto, M., 2009. Occurrence of peritrich ciliates on the limnic oligochaete Limnodrilus hoffmeisteri (Oligochaeta, Tubificidae) in the neotropics. J. Nat. Hist. 43(1-2), 1-15. http://doi.org/10.1080/00222930802478644.

Fernandez-Leborans, G., & Tato-Porto, M.L., 2000. A review of the species of protozoan epibionts on crustaceans. I. Peritrich ciliates. Crustaceana 73(6), 643-683. http://doi.org/10.1163/156854000504705.

Fernandez-Leborans, G., 2009. A Review of Recently Described Epibioses of Ciliate Protozoa on Crustacea. Crustaceana 82(2), 167-189. http://doi.org/10.1163/156854008X367223.

Green, J., 1974. Parasites and epibionts of Cladocera. Trans. Zool. Soc. Lond. 32(6), 417-515. http://doi.org/10.1111/j.1096-3642.1974.tb00031.x.

Haney, J.F., & Hall, D.J., 1973. Sugar‐coated Daphnia: a preservation technique for Cladocera. Limnol. Oceanogr. 18(2), 331-333. http://doi.org/10.4319/lo.1973.18.2.0331.

Henebry, M.S., & Ridgeway, B.T., 1979. Epizoic ciliated protozoa of planktonic copepods and cladocerans and their possible use as indicators of organic pollution. Trans. Am. Microsc. Soc. 98(4), 495-508. http://doi.org/10.2307/3225899.

Hunter, J.D., 2007. Matplotlib: A 2D graphics environment. Comput. Sci. Eng. 9(3), 90-95. http://doi.org/10.1109/MCSE.2007.55.

Jones, S., Carrasco, N.K., Perissinotto, R., & Vosloo, A., 2016. Association of the epibiont Epistylis sp. with a calanoid copepod in the St Lucia Estuary, South Africa. J. Plankton Res. 38(6), 1404-1411. https://doi.org/10.1093/plankt/fbw069.

Jones, S., Carrasco, N.K., Vosloo, A., & Perissinotto, R., 2018. Impacts of turbidity on an epibiotic ciliate in the St Lucia Estuary, South Africa. Hydrobiologia 815(1), 37-46. http://doi.org/10.1007/s10750-018-3545-8.

Josué, I.I., Sodré, E.O., Setubal, R.B., Cardoso, S.J., Roland, F., Figueiredo‐Barros, M.P., & Bozelli, R.L., 2021. Zooplankton functional diversity as an indicator of a long‐term aquatic restoration in an Amazonian lake. Restor. Ecol. 29(5), e13365. http://doi.org/10.1111/rec.13365.

Kumar, R., Kumari, S., Malika, A., Sharma, A.P., & Dahms, H.U., 2022. Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod. Sci. Rep. 12(1), 22631. PMid:36587046. http://doi.org/10.1038/s41598-022-26004-5.

Medlin, L., Elwood, H.J., Stickel, S., & Sorgin, M.L., 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71(2), 491-499. PMid:3224833. http://doi.org/10.1016/0378-1119(88)90066-2.

Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens M.H.M., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H.B.A., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M.O., Lahti, L., McGlinn, D., Ouellette, M.H., Cunha, E.R., Smith, T., Stier, A., Ter Braak, C.J.F., & Weedon, J., 2020. Vegan: Community Ecology Package. R package version 2.6-8 [online]. Retrieved in 2024, June 29, from https://CRAN.R-project.org/package=vegan.

Regali-Seleghim, M.H., & Godinho, M.J., 2004. Peritrich epibiont protozoans in the zooplankton of a subtropical shallow aquatic ecosystem (Monjolinho Reservoir, São Carlos, Brazil). J. Plankton Res. 26(5), 501-508. http://doi.org/10.1093/plankt/fbh055.

Santos, G.S., Ibraim, V.R.C., Silva, E.E.C., & Eskinazi-Sant’Anna, E.M., 2020. Interaction between Epistylis sp. and copepods in tropical lakes: responses of epibiont infestation to species host density. Limnologica 84, 125815. http://doi.org/10.1016/j.limno.2020.125815.

Seabold, J., & Perktold, J., 2010. Statsmodels: econometric and statistical modeling with Python. In: Proceedings of the 9th Python in Science Conference, Austin: Scipy.org, 57-61. http://doi.org/10.25080/Majora-92bf1922-011.

Souissi, A., Souissi, S., & Hwang, J., 2013. The effect of epibiont ciliates on the behavior and mating success of the copepod Eurytemora affinis. J. Exp. Mar. Biol. Ecol. 445, 38-43. http://doi.org/10.1016/j.jembe.2013.04.002.

Souza, P.M., Dias, R.J.P., Loures, A., Rossi, M.F., Amato, J.F.R., & D’Agosto, M., 2024. High infestation and phylogenetic position of Epistylis sp.(Ciliophora, Peritrichia) on Aegla serrana Buckup & Rossi (Crustacea, Anomura) from southern Brazil. An. Acad. Brasil. Ciênc. 96(1), e20230739. https://doi.org/10.1590/0001-3765202420230739.

Thomaz, S.M., Bini, L.M., & Bozelli, R.L., 2007. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579(1), 1-13. http://doi.org/10.1007/s10750-006-0285-y.

Utz, L.R.P., & Coats, W., 2005. The role of motion in the formation of free-living stages e attachment of the peritrich epibiont Zoothamnium intermedium (Ciliophora, Peritrichia). Biociencias 13, 69-74.

Wahl, M., 1989. Marine Epibiosis. I. Fouling and antifouling: some basic aspects. Mar. Ecol. Prog. Ser. 58, 175-189. http://doi.org/10.3354/meps058175.

Wahl, M., 2008. Ecological lever and interface ecology: epibiosis modulates the interactions between host e environment. Biofouling 24(6), 427-438. PMid:18686057. http://doi.org/10.1080/08927010802339772.

Waskom, M., 2021. Seaborn: statistical data visualization. J. Open Source Softw. 6(60), 3021. http://doi.org/10.21105/joss.03021.

Xu, Z., & Burns, C.W., 1991. Effects of the epizoic ciliate, Epistylis daphniae on growth, reproduction and mortality of Boekella triarticulata (Thomson) (Copepoda: calanoida). Hydrobiologia 209(3), 183-189. http://doi.org/10.1007/BF00015341.

Xu, Z., 1992. The abundance of epizoic ciliate Epistylis daphniae related to their Moina macrocopa in an urban stream. J. Invertebr. Pathol. 60(2), 197-200. http://doi.org/10.1016/0022-2011(92)90097-N.
 


Submetido em:
29/06/2024

Aceito em:
14/10/2024

Publicado em:
05/12/2024

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