Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X4221
Acta Limnologica Brasiliensia
Original Article

Factors stimulating the hatching of resting eggs and their contribution to the composition of cladoceran assemblages in tropical temporary lagoons

Fatores que estimulam a eclosão de ovos de resistência e a sua contribuição para a composição das assembleias de cladóceros em lagoas temporárias tropicais

Wesley Luiz Guimarães; Eliana Aparecida Panarelli; Natan Guilherme dos Santos; Maria Stela Maioli Castilho-Noll

http://dx.doi.org/10.1590/S2179-975X4221 Acta Limnol. Bras. (Online), vol.36, e28, 2024
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Abstract

Aim: We aimed to verify the contribution of cladocerans’ resting eggs to the active communities of temporary lagoons and, through an experiment, identify which conditions induce high hatching rates.

Methods: Cladocera assemblages were sampled in four temporary lagoons in the Turvo River floodplain (20° 22’S and 49° 16’W), in the northwest region of São Paulo State, Brazil. Sediment samples were taken during the dry season from a depth of 5 cm, using a 4.5 cm diameter corer. Plankton samples were taken from the water column before and after the dry season. For the hatching test, two treatments were performed 1. Natural condition – without light and temperature control; 2. Controlled condition – with controlled photoperiod and temperature. Temperature, pH, conductivity, dissolved oxygen and hatching of resting eggs were monitored for two weeks. The influence of the parameters on hatching in both treatments was evaluated using Hierarchical Partition Analysis.

Results: Hatching of resting eggs was higher in the Controlled condition than in the Natural one. Thirty percent of species observed in the active community after flooding hatched in the laboratory test. Conductivity, pH, and dissolved oxygen were positively correlated to the hatching of some species, e.g., Ephemeroporus hybridus, Leydigiops ornata, Notoalona sculpta and Ilyocryptus spinifer. The first species to hatch were those living associated with macrophytes and at low depths.

Conclusions: Our results show that stable temperature and photoperiod with similar light and dark hours stimulate greater hatching of Cladocera resting eggs. Variables such as pH, conductivity and dissolved oxygen were also correlated with the hatching of some species. We observed that the first contributions to activating the community after drought came from hatching of species usually associated with macrophytes and low depth conditions.

Keywords

dormant community, sediment, ephippium, flood plain, experiment

Resumo

Objetivo: Este estudo tem como objetivo verificar a contribuição dos ovos de resistência de cladóceros para as comunidades ativas de lagoas temporárias e testar experimentalmente as condições específicas para a eclosão destes ovos de resistência.

Métodos: Amostras de cladóceros foram obtidas em quatro lagoas temporárias na planície de inundação do rio Turvo (20° 22’S e 49° 16’W), na região noroeste do Estado de São Paulo, Brasil. Amostras de 5 cm de sedimento foram coletadas durante a estação seca, usando um corer de 4,5 cm de diâmetro. Amostras de plâncton foram coletadas antes e depois da estação seca. Para o teste de incubação, foram realizados dois tratamentos a saber, 1. Condições naturais - sem controle de luz e temperatura; 2. Condições controladas - com fotoperíodo e temperatura controlados. A condição da água e a eclosão dos ovos de resistência foram monitoradas por duas semanas. A influência dos parâmetros na eclosão em ambos os tratamentos foi avaliada por meio da Análise de Partição Hierárquica.

Resultados: A eclosão dos ovos de resistência foi maior no tratamento Condições controladas do que Condições naturais. Trinta por cento das espécies observadas na comunidade ativa após o alagamento eclodiram no teste de laboratório. Condutividade, pH e oxigênio dissolvido foram positivamente correlacionados com a eclosão de algumas espécies como Ephemeroporus hybridus, Leydigiops ornata, Notoalona sculpta e Ilyocryptus spinifer. As primeiras espécies a eclodirem foram aquelas associadas a macrófitas e em ambients com baixas profundidades.

Conclusões: Nossos resultados mostram que condições constantes de temperatura e fotoperíodo estimulam maior taxa de eclosão dos ovos de resistência de Cladocera. Variáveis como pH, condutividade e oxigênio dissolvido também foram correlacionados com a eclosão de algumas espécies estudadas. Observamos que as primeiras contribuições para a comunidade ativa após a seca vieram da eclosão de espécies geralmente associadas a macrófitas e condições de baixa profundidade.

Palavras-chave

comunidade dormente, sedimento, efípio, planície de inundação, experimento

References

Alvares, C.A., Stape, J.L., Sentelhas, P.C., Moraes, G., Leonardo, J., & Sparovek, G., 2013. Köppen’s climate classification map for Brazil. Meteorol. Z. 22(6), 711-728. http://doi.org/10.1127/0941-2948/2013/0507.

Araújo, L.R., Lopes, P.M., Santangelo, J.M., Petry, A.C., & Bozelli, R.L., 2013. Zooplankton resting egg banks in permanent and temporary tropical aquatic systems. Acta Limnol. Bras. 25(3), 235-245. http://doi.org/10.1590/S2179-975X2013000300004.

Battauz, Y.S., De Paggi, S.B.J., & Paggi, J.C., 2017. Macrophytes as dispersal vectors of zooplankton resting stages in a subtropical riverine floodplain. Aquat. Ecol. 51(2), 191-201. http://doi.org/10.1007/s10452-016-9610-3.

Brendonck, L., 1996. Diapause, quiescence, hatching requirements: what we can learn from large freshwater branchiopods (Crustacea: Branchiopoda: Anostraca, Notostraca, Conchostraca). Hydrobiologia 320(1-3), 85-97. http://doi.org/10.1007/BF00016809.

Brendonck, L., Pinceel, T., & Ortells, R., 2017. Dormancy and dispersal as mediators of zooplankton population and community dynamics along a hydrological disturbance gradient in inland temporary pools. Hydrobiologia 796(1), 201-222. http://doi.org/10.1007/s10750-016-3006-1.

Cáceres, C.E., & Tessier, A.J., 2004. To sink or swim: variable diapause strategies among Daphnia species. Limnol. Oceanogr. 49(4part2), 1333-1340. http://doi.org/10.4319/lo.2004.49.4_part_2.1333.

Chevan, A., & Sutherland, M., 1991. Hierarchical partitioning. Am. Stat. 45(2), 90-96. http://doi.org/10.1080/00031305.1991.10475776.

Coelho, P.N., Paes, T.A.S.V., Maia-Barbosa, P.M., & Santos-Wisniewski, M.J., 2021. Effects of pollution on dormant-stage Banks of cladocerans and rotifers in a large tropical reservoir. Environ. Sci. Pollut. Res. Int. 28(24), 30887-30897. PMid:33594550. http://doi.org/10.1007/s11356-021-12751-x.

Coronel, J.S., Aguilera, X., Decleck, S., & Brendock, L., 2009. Resting egg bank reveals high cladoceran species richness in high-altitude temporary peat land pools. Revi. Boliv. Ecol. Conserva. Amb. 25, 51-67.

Crispim, M.C., & Watanabe, T., 2001. What can dry reservoir sediments in a semi-arid region in Brazil tell us about cladocera? Hydrobiologia 42(1-3), 101-105. http://doi.org/10.1023/A:1017550603022.

De Stasio Junior, B.T., 1990. The role of dormancy and emergence patterns in the dynamics of a freshwater zooplankton community. Limnol. Oceanogr. 35(5), 1079-1090. http://doi.org/10.4319/lo.1990.35.5.1079.

Dias, J.D., Simões, N.R., Meerhoff, M., Lansac-Tôha, F.A., Velho, L.F.M., & Bonecker, C.C., 2016. Hydrological dynamics drives zooplankton metacommunity structure in a Neotropical floodplain. Hydrobiologia 781(1), 109-125. http://doi.org/10.1007/s10750-016-2827-2.

Elmoor-Loureiro, L.M.A., 1997. Manual de identificação dos Cladóceros Límnicos do Brasil. Brasília: Universa.

Fox, J., & Weisberg, S., 2011. Multivariate linear models in R: an R companion to applied regression. Los Angeles: Thousand Oaks.

Freiry, R.F., Pires, M.M., Gouvea, A., Hoffman, P.H.O., Stenert, C., & Maltchik, L., 2021. Ecological correlates of the alpha and beta diversity of zooplankton hatchling communities in seasonal subtropical ponds. Ecol. Res. 36(3), 464-477. http://doi.org/10.1111/1440-1703.12213.

Fryer, G., 1968. Evolution and adaptive radiation in the Chydoridae (Crustacea: Cladocera): a study in comparative functional morphology and ecology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 254(795), 221-384. http://doi.org/10.1098/rstb.1968.0017.

Gerhard, M., Iglesias, C., Clemente, J.M., Goyenola, G., Meerhoff, M., Pacheco, J.P., Mello, F.T., & Mazzeo, N., 2017. What can resting egg bank tell about cladoceran diversity in a shallow subtropical lake? Hydrobiologia 798(1), 75-86. http://doi.org/10.1007/s10750-016-2654-5.

Golterman, H.L., Clymo, R.S., & Ohmstad, M.A.A., 1978. Methods for physical and chemical analysis of freshwaters. Oxford: Blackwell Scientific Publication.

Hairston Junior, N.G., & Cáceres, C.E., 1996. Distribution of crustacean diapause: micro-and macroevolutionary pattern and process. Hydrobiologia 320(1-3), 27-44. http://doi.org/10.1007/BF00016802.

Havel, J.E., Eisenbacher, E.M., & Black, A.A., 2000. Diversity of crustacean zooplankton in riparian wetlands: colonization and egg banks. Aquat. Ecol. 34(1), 63-76. http://doi.org/10.1023/A:1009918703131.

Iglesias, C., Bonecker, C., Brandao, L., Crispim, M.C., Eskinazi‐Sant’anna, E.M., Gerhard, M., Portinho, J.L., Maia-Barbosa, P., Panarelli, E., & Santangelo, J.M., 2016. Current knowledge of South American cladoceran diapause: A brief review. Int. Rev. Hydrobiol. 101(3-4), 91-104. http://doi.org/10.1002/iroh.201501825.

Jones, N.T., & Gilbert, B., 2016. Changing climate cues differentially alter zooplankton dormancy dynamics across latitudes. J. Anim. Ecol. 85(2), 559-569. PMid:26590065. http://doi.org/10.1111/1365-2656.12474.

La, G.H., Jeong, H.G., Kim, M.C., Joo, G.J., Chang, K.H., & Kim, H.W., 2009. Response of diapausing eggs hatching to changes in temperature and the presence of fish kairomones. Hydrobiologia 63(1), 399-402. http://doi.org/10.1007/s10750-009-9913-7.

Lass, S., Vos, M., Wolinska, J., & Spaak, P., 2005. Hatching with the enemy: daphnia diapausing eggs hatch in the presence of fish kairomones. Chemoecology 15(1), 7-12. http://doi.org/10.1007/s00049-005-0286-8.

Lopes, P.M., Bozelli, R., Bini, L.M., Santangelo, J.M., & Declerck, S.A., 2016. Contributions of airborne dispersal and dormant propagule recruitment to the assembly of rotifer and crustacean zooplankton communities in temporary ponds. Freshw. Biol. 61(5), 658-669. http://doi.org/10.1111/fwb.12735.

Mac Nally, R., 2002. Multiple regression and inference in ecology and conservation biology, Further comments on identifying important predictor variables. Biodivers. Conserv. 11(8), 1397-1401. http://doi.org/10.1023/A:1016250716679.

Maia‐Barbosa, P.M., Eskinazi‐Sant’anna, E.M., Valadares, C.F., & Pessoa, G.C.D., 2003. The resting eggs of zooplankton from a tropical, eutrophic reservoir (Pampulha Reservoir, south‐east Brazil). Lakes Reservoirs: Res. Manage. 8(3-4), 269-275. http://doi.org/10.1111/j.1440-1770.2003.00229.x.

Melo, D.A.S., Santos-Wisniewski, M.J., Batista, H.M., & Engel, G.M., 2022. Zooplankton resting egg Banks as a strategy to maintain diversity in a small tropical reservoir ecosystem. Pan-Am. J. Aquat. Sci. 17(3), 217-227. http://doi.org/10.54451/PanamJAS.17.3.217.

Morais-Júnior, C.S., Diniz, L.P., Golçalves-Souza, T., Elmoor-Loureiro, L.M.A., & Melo Junior, M., 2019. Bird feet morphology drives the dispersal of rotifers and microcrustaceans in a Neotropical temporary pond. Aquat. Sci. 81(4), 1-9. http://doi.org/10.1007/s00027-019-0666-8.

Nielsen, D.L., Jasper, E.W., Ning, N., & Lawler, S., 2015. High sediment temperatures influence the emergence of dormant aquatic biota. Mar. Freshw. Res. 66(12), 1138-1146. http://doi.org/10.1071/MF14272.

Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.N., & Wagner, H., 2013. Vegan: community ecology package. R package version 2.2-0. Vienna: R Foundation for Statistical Computing. Retrieved in 2021, June 14, from https://cran.r-project.org/web/packages/vegan/index.html

Paes, T.A., Rietzler, A.C., Pujoni, D.G., & Maia-Barbosa, P.M., 2016. High temperatures and absence of light affect the hatching of resting eggs of Daphnia in the tropics. An. Acad. Bras. Cienc. 88(1), 179-186. http://doi.org/10.1590/0001-3765201620140595.

Palazzo, F., Bonecker, C.C., & Fernandes, A.P.C., 2008a. Resting cladoceran eggs and their contribution to zooplankton diversity in a lagoon of the Upper Paraná River floodplain. Lakes Reservoirs: Res. Manage. 13(3), 207-214. http://doi.org/10.1111/j.1440-1770.2008.00370.x.

Palazzo, F., Bonecker, C.C., & Nagae, M.Y., 2008b. Zooplankton dormancy forms in two environments of the upper Paraná River floodplain (Brazil). Acta Limnol. Bras. 20, 55-62.

Panarelli, E.A., Casanova, S.M.C., & Henry, R., 2008. The role of resting eggs in the recovery of zooplankton community in a marginal lake of the Paranapanema River (São Paulo, Brazil), after a long drought period. Acta Limnol. Bras. 20, 73-88.

Panarelli, E.A., Nielsen, D.L., & Holland, A., 2021. Cladocera resting egg banks in temporary and permanent wetlands. J. Limnol. 80(1), 1971-1983. http://doi.org/10.4081/jlimnol.2020.1971.

Portinho, J.L., Nielsen, D.L., Daré, L., Henry, R., Oliveira, R.C., & Branco, C.C.Z., 2018. Mixture of comercial hervicides based on 2,4-D and glyphosate mixture can suppress the emergence of zooplankton from sediments. Chemosphere 203, 151-159. PMid:29614408. http://doi.org/10.1016/j.chemosphere.2018.03.156.

Portinho, J.L., Oliveira, H.N., & Branco, C.C.Z., 2021. Resting egg banks can facilitate recovery of zooplankton communities after short exposure to glyphosate. Ecotoxicology 30(3), 492-501. PMid:33649983. http://doi.org/10.1007/s10646-021-02371-z.

R Development Core Team, 2014. R: a language and environment for statistical computing (Online). Vienna: R Foundation for Statistical Computing. Retrieved in 2021, June 14, from https://www.gbif.org/pt/tool/81287/r-a-language-and-environment-for-statistical-computing

Ranga, N.T., Rezende, A.A., Cavasan, O., Toniato, M.T.Z., Cielo-Filho, R., & Stranghetti, V., 2012. Caracterização florística de remanescentes de vegetação nativa da região noroeste do estado de São Paulo. Fauna e Flora de fragmentos florestais remanescentes da região Noroeste do Estado de São Paulo. In: Necchi Junior, O., ed. Fauna e flora de fragmentos florestais remanescentes da região noroeste do Estado de São Paulo. Ribeirão Preto: Holos Editora, 105-135.

Rojas, N.E.T., Marins, M.A., & Rocha, O., 2001. The effect of abiotic factors on the hatching of Moina micrura Kurz, 1874 (Crustacea: Cladocera) ephippial eggs. Brazil. Braz. J. Biol. 61(3), 371-376. PMid:11706563. http://doi.org/10.1590/S1519-69842001000300005.

Sacherová, V., & Hebert, P.D., 2003. The evolutionary history of the Chydoridae (Crustacea: cladocera). Biol. J. Linn. Soc. Lond. 79(4), 629-643. http://doi.org/10.1046/j.1095-8312.2003.00216.x.

Santangelo, J.M., Esteves, F.A., Manca, M., & Bozelli, R.L., 2014. Disturbances due to increased salinity and the resilience of zooplankton communities: the potential role of the resting egg bank. Hydrobiologia 722, 103-113. http://doi.org/10.1007/s10750-013-1683-6.

Santangelo, J.M., 2009. Produção, eclosão e implicações ecológicas e evolutivas dos estágios dormentes do zooplâncton. Limnotemas 7, 1-26.

Santangelo, J.M., Lopes, P.M., Nascimento, M.O., Fernandes, A.P.C., Bartole, S., Figueiredo-Barros, M.P., Leal, J.J.F., Esteves, F.D.A., Farjalla, V.F., Bonecker, C.C., & Bozelli, R.L., 2015. Community structure of resting egg banks and concordance patterns between dormant and active zooplankters in tropical lakes. Hydrobiologia 758, 183-195. http://doi.org/10.1007/s10750-015-2289-y.

Schwartz, S.S., & Hebert, P.D., 1987. Methods for the activation of the resting eggs of Daphnia. Freshw. Biol. 17(2), 373-379. http://doi.org/10.1111/j.1365-2427.1987.tb01057.x.

Sousa, F.D.R., & Elmoor-Loureiro, L.M.A., 2019. Identification key for the Brazilian genera and species of Aloninae (Crustacea, Branchiopoda, Anomopoda, Chydoridae). Pap. Avulsos Zool. 59, e20195924. http://doi.org/10.11606/1807-0205/2019.59.24.

Souza-Santos, G., Silva, E.E.C., Balmant, F.M., Gomes, P.C.S., & Eskinazi-Sant’Anna, E.M., 2021. Impacts of exposure to mine tailings on zooplankton hatching from a resting egg bank. Aquat. Ecol. 55(2), 545-557. http://doi.org/10.1007/s10452-021-09844-7.

Stephan, L.R., Castilho-Noll, M.S.M., & Henry, R., 2017. Comparison among zooplankton communities in hydrologically different lentic ecosystems. Limnetica 36, 99-112. http://doi.org/10.23818/limn.36.08.

Teixeira, C., & Kutner, M.B., 1962. Plankton studies in a mangrove environment I first assessment of standing stock and ecological factors. Bol. Inst. Oceanogr. 12(3), 101-124. http://doi.org/10.1590/S0373-55241962000300006.

Vandekerkhove, J., Declerck, S., Brendonck, L., Conde-Porcuna, J.M., Jeppesen, E., & De Meester, L.D., 2005a. Hatching of cladoceran resting eggs: temperature and photoperiod. Freshw. Biol. 50(1), 96-104. http://doi.org/10.1111/j.1365-2427.2004.01312.x.

Vandekerkhove, J., Declerck, S., Jeppesen, E., Conde-Porcuna, J.M., Brendonck, L., & De Meester, L., 2005b. Dormant propagule banks integrate spatio-temporal heterogeneity in cladoceran communities. Oecologia 142(1), 109-116. PMid:15378346. http://doi.org/10.1007/s00442-004-1711-3.

Vargas, A.L., Santangelo, J.M., & Bozelli, R.L., 2022. Hatching under brownification: DOC-mediated changes in physical, but not chemical properties of water affect hatching patterns of Cladocera resting eggs. Environ. Sci. Pollut. Res. Int. 29(42), 64124-64131. PMid:35471758. http://doi.org/10.1007/s11356-022-19864-x.

Vendramin, D., Pires, M.M., Medeiros, E.S.F., Stenert, C., & Maltchik, L., 2023. Life finds a way: hatching dynamics of zooplankton dormant stages in intermittent wetlands from the Brazilian tropical semiarid. J. Arid Environ. 212, 104949. http://doi.org/10.1016/j.jaridenv.2023.104949.

Walsh, C., & Mac Nally, R., 2012. Hier part, hierarchical partitioning R package version 10-3 (Online). Vienna: R Foundation for Statistical Computing. Retrieved in 2021, June 14, from http://CRAN.R-project.org/package=hier.part

Waterkeyn, A., Vanschoenwinkel, B., Vercampt, H., Grillas, P., & Brendonck, L., 2011. Long‐term effects of salinity and disturbance regime on active and dormant crustacean communities. Limnol. Oceanogr. 56(3), 1008-1022. http://doi.org/10.4319/lo.2011.56.3.1008.

Walsh, E.J., Smith, H.A., & Wallace, R.L., 2014. Rotifers of temporary waters. Int. Rev. Hydrobiol. 99(1-2), 3-19. http://doi.org/10.1002/iroh.201301700.

Warnes, G.R., Bolker, B., & Lumley, T., 2013. gplots: Various R Programming Tools for Plotting Data. R package version 300. (Online). Vienna: R Foundation for Statistical Computing. Retrieved in 2021, June 14, from https://cran.r-project.org/web/packages/gplots/index.html
 

Submitted date:
06/14/2021

Accepted date:
06/17/2024

Publication date:
08/22/2024

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