Ecotoxicological investigation of cyanobacterial crude extracts to Daphnia magna under subchronic test conditions

Ecotoxicological investigation of cyanobacterial crude extracts to Daphnia magna under subchronic test conditions

Cyanobacterial blooms often consist of mixtures of microcystin-producing and microcystin-free species, and both can cause unpredictable effects on aquatic organisms. In this work, the subchronic effects of the cyanobacterial crude extracts (CCEs) from microcystin-producing and microcystin-free cyanobacteria with different microcystin concentrations (1, 10, and 50 mu gL(-1))on Daphnia magna were investigated. The life-history trait responses of D. magna to CCEs were determined based on survival, reproduction, and somatic growth. In addition, the physiological response, represented by the feeding rate of D. magna on green algae (Scenedesmus sp.), after exposure to both types of crude extracts was estimated. Our results showed that both microcystin-containing (MCCE) and microcystin-free (NCCE) crude extracts insignificantly reduced survival but strongly enhanced reproduction and somatic growth of organisms. However, degradation of eggs and neonates of the gravid females exposed to CCEs was observed. In addition, the feeding rate of D. magna exposed to MCCE increased significantly, whereas no change in the feeding rate was observed for NCCE-exposed D. magna. In general, new and interesting aspects of the toxicity of MCCE and NCCE were revealed by this study, which contributes to the understanding of the toxicity of Pseudanabaena sp. extract on D. magna under bioassays.

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  • Bednarska A, Slusarczyk M (2013). Effect of non-toxic, filamentous cyanobacteria on egg abortion in Daphnia under various thermal conditions. Hydrobiologia 715: 151-157. doi:10.1007/ s10750-012-1424-2
  • Bláha L, Babica P, Maršálek B (2009). Toxins produced in cyanobacterial water blooms–toxicity and risks. Interdisciplinary Toxicology 2 (2): 36-41. doi:10.2478/v10102-009-0006-2
  • Campos B, Altenburger R, Gómez C, Lacorte S, Pina B et al. (2014). First evidence for toxic defense based on the multixenobiotic resistance (MXR) mechanism in Daphnia magna. Aquatic Toxicology 148: 139-151. doi:10.1016/j.aquatox.2014.01.001
  • Chen W, Song L, Ou D, Gan N (2005). Chronic toxicity and responses of several important enzymes in Daphnia magna on exposure to sublethal microcystin-LR. Environmental Toxicology 20 (3): 323-330. doi:10.1002/tox.20108
  • Chorus I, Bartram J (editors) (1999). Toxic Cyanobacteria in water: A guide to their public health consequences, monitoring and management. London, UK: E & FN Spon (on behalf of World Health Organisation) Press.
  • Cooke GN, Welch EB, Peterson SA, Nichols SA (editors) (2005). Restoration and management of lakes and reservoirs. 3rd ed. Boca Raton, USA: CRC Press.
  • Cui F, Chai T, Liu X, Wang C (2016). Toxicity of three strobilurins (kresoxim-methyl, pyraclostrobin, and trifloxystrobin) on Daphnia magna. Environmental Toxicology and Chemistry 36 (1): 182-189. doi:10.1002/etc.3520
  • da Costa SM, Ferrão-Filho AS, Azevedo SMFO (2013). Effects of saxitoxin- and non-saxitoxin-producing strains of the cyanobacterium Cylindrospermopsis raciborskii on the fitness of temperate and tropical cladocerans. Harmful Algae 28: 55-63. doi:10.1016/j.hal.2013.05.017
  • Dao TS, Do-Hong LC, Wiegand C (2010). Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55 (7): 1244-1254. doi:10.1016/j.toxicon.2010.01.014
  • Dao TS, Le TH, Pham TL, Do-Hong LC, Nguyen PD (2014). Influences of cyanobacterial toxins microcystins on the seedling of plants. Journal of Environmental Protection 05 (01): 35-41. doi:10.4236/jep.2014.51005
  • Dao TS, Ortiz-Rodriguez R, Do-Hong LC, Wiegand C (2013a). Non-microcystin and non-cylindrospermopsin producing cyanobacteria affect the biochemical responses and behavior of Daphnia magna. International Review of Hydrobiology 98 (5): 235-244. doi:10.1002/iroh.201301626
  • .Dao TS, Tran TL, Pham TL, Do-Hong LC, Nguyen PD (2013b). Impacts of cyanobacterial toxins from Dau Tieng Reservoir, Vietnam, on the early life stage of zebrafish. In: 4th International Conference on Biology, Environment and Chemistry; Singapore, IPCBEE, 58: 41-46.
  • Dao TS, Vo TM, Wiegand C, Bui BT, Dinh KV (2018). Transgenerational effects of cyanobacterial toxins on a tropical micro-crustacean Daphnia lumholtzi across three generations. Environmental Pollution 243 (Pt B): 791-799. doi:10.1016/j. envpol.2018.09.055
  • Díez-Quijada L, Prieto AI, Puerto M, Jos Á, Cameán AM (2019). In Vitro mutagenic and genotoxic assessment of a mixture of the cyanotoxins microcystin-LR and cylindrospermopsin.Toxins (Basel) 11 (6), pii: E318. doi:10.3390/toxins11060318
  • Dionisio Pires LM, Bontes BM, Van Donk E, Ibelings BW (2005). Grazing on colonial and filamentous, toxic and non-toxic cyanobacteria by the zebra mussel Dreissenapolymorpha. Journal of Plankton Research 27 (4): 331-339. doi:10.1093/ plankt/fbi008
  • Epel D, Luckenbach T, Stevenson CN, Macmanus-Spencer LA, Hamdoun A et al. (2008). Efflux transporters: newly appreciated roles in protection against pollutants. Environmental Science & Technology 42 (11): 3914-3920. doi:10.1021/es087187v
  • Ferrando MD, Janssen C, Andreu E, Persoone G (1993). Ecotoxicological studies with the freshwater rotifer Brachionuscalyciflorus III. The effects of chemicals on feedingbehavior. Ecotoxicology and Environmental Safety 26 (1): 1-9. doi:10.1006/eesa.1993.1035
  • Ferrao-Filho AS, Azevedo SMFO, Demott WR (2000). Effects of toxic and non-toxic cyanobacteria on the lifehistory of tropical and temperate cladocerans. Freshwater Biology 45 (1): 1-19. doi:10.1046/j.1365-2427.2000.00613.x
  • Gauld T (1951). The grazing rate of marine copepods. Journal of the Marine Biological Association of the United Kingdom 29 (3): 695-706. doi:10.1017/S0025315400052875
  • Ghadouani A, Pinel-Alloul B, Plath K, Codd GA, Lampert W (2004). Effects of Microcystis aeruginosa and purified microcystin-LR on the feeding behavior of Daphnia pulicaria. Limnology and Oceanography 49 (3): 666-679. doi:10.4319/lo.2004.49.3.0666
  • Guzmán-Guillén R, Puerto M, Gutiérrez-Praena D, Prieto AI, Pichardo S et al. (2017). Potential use of chemoprotectants against the toxic effects of cyanotoxins: A review. Toxins (Basel) 9 (6): 175. doi:10.3390/toxins9060175
  • Herrera N, Palacio J, Echeverri F, Ferrão-Filho A (2014). Effects of a cyanobacterial bloom sample containing microcystin-LR on the ecophysiology of Daphnia similis. Toxicology Reports 1: 909-914. doi:10.1016/j.toxrep.2014.10.017
  • Herrera NA, Echeverri LF, Ferrão-Filho AS (2015). Effects of phytoplankton extracts containing the toxin microcystin-LR on the survival and reproduction of cladocerans. Toxicon 95 (2015): 38-45. doi:10.1016/j.toxicon.2014.12.016
  • Hulot FD, Carmignac D, Legendre S, Yéprémian C, Bernard C (2012). Effects of microcystin-producing and microcystin-free strains of Planktothrixagardhii on long-term population dynamics of Daphnia magna. Annales de Limnologie - International Journal of Limnology 48 (3): 337-347. doi:10.1051/limn/2012023
  • Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998). Combo: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377 (1): 147-159. doi:10.1023/A:1003231628456
  • Lau NS, Matsui M, Abdullah AAA (2015). Cyanobacteria: photoautotrophic microbial factories for the sustainable synthesis of industrial products. Journal of Biomedicine and Biotechnology 2015 (2): 754934. doi:10.1155/2015/754934
  • Liang Y, Ouyang K, Chen X, Su Y, Yang J (2017). Life strategy and grazing intensity responses of Brachionuscalyciflorus fed on different concentrations of microcystin-producing and microcystin-free Microcystis aeruginosa. Scientific Reports 7: 43127. doi:10.1038/srep43127
  • Lurling M (2003). Effects of microcystin-free and microcystincontaining strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna. Environmental Toxicology 18 (3): 202-210. doi:10.1002/tox.10115
  • Meyer JS, Ingersoll CG, Mcdonald LL, Boyce MS (1986). Estimating uncertainty in population growth rates: Jacknife vs. Bootstrap techniques. Ecology 67 (5): 1156-1166. doi:10.2307/1938671
  • OECD (2012). Guideline for the Testing of Chemicals No 211. Daphnia magna Reproduction Test. Organization for Economic Cooperation and development, Paris, p. 202.
  • Okumura DT, Sotero-Santos RB, Takenaka RA, Rocha O (2007). Evaluation of cyanobacteria toxicity in tropical reservoirs using crude extracts bioassay with cladocerans. Ecotoxicology 16 (2): 263-270. doi:10.1007/s10646-006-0126-9
  • Ortiz-Rodríguez R, Dao TS, Wiegand C (2012). Transgenerational effects of microcystin-LR on Daphnia magna. The Journal of Experimental Biology 215 (Pt 16): 2795-2805. doi:10.1242/ jeb.069211
  • Ortiz-Rodríguez R, Wiegand C (2010). Age related acute effects of microcystin-LR on Daphnia magna biotransformation and oxidative stress. Toxicon 56 (8): 1342-1349. doi:10.1016/j. toxicon.2010.07.020
  • Pawlik-Skowrońska B, Toporowska M, Mazur-Marzec H (2019). Effects of secondary metabolites produced by different cyanobacterial populations on the freshwater zooplankters Brachionuscalyciflorus and Daphnia pulex. Environmental Science and Pollution Research 26: 11793-11804. doi:10.1007/ s11356-019-04543-1
  • Pham TL, Dao TS, Shimizu K, Do-Hong LC, Utsumi M (2015b). Isolation and characterization of microcystin-producing cyanobacteria from Dau Tieng Reservoir, Vietnam. Nova Hedwigia 101 (1-2): 3-20. doi:10.1127/nova_ hedwigia/2014/0243
  • Pham TL, Ngo XQ (2017). Detection of potentially toxigenic microcystis strains from Dau Tieng Reservoir. Journal of Biotechnology 15 (4): 745-752. doi:10.15625/1811- 4989/15/4/13418
  • Pham TL, Shimizu K, Dao TS, Hong-Do LC, Utsumi M (2015a). Microcystin uptake and biochemical responses in the freshwater clam Corbicula leana P. exposed to toxic and non-toxic Microcystis aeruginosa: Evidence of tolerance to cyanotoxins. Toxicology Reports 2: 88-98. doi:10.1016/j. toxrep.2015.01.012
  • Pham TL, Shimizu K, Dao TS, Motoo U (2017). First report on free and covalently bound microcystins in fish and bivalves from Vietnam: Assessment of risks to humans. Environmental Toxicology and Chemistry 36 (11): 2953-2957. doi:10.1002/ etc.3858
  • Pham TL, Shimizu K, Kanazawa A, Gao Y, Dao TS et al. (2016). Microcystin accumulation and biochemical responses in the edible clam Corbiculaleana P. exposed to cyanobacterial crude extract. Journal of Environmental Sciences 44: 120-130. doi:10.1016/j.jes.2015.09.018
  • Pietsch C, Wiegand C, Ame MV, Nicklisch A, Wunderlin D et al. (2001). The effects of cyanobacterial crude extract on different aquatic organisms: Evidence for cyanobacterial toxin modulating factors. Environmental Toxicology 16 (6): 535- 542. doi:10.1002/tox.10014
  • Puerto M, Pichardo S, Jos A, Cameán AM (2009). Comparison of the toxicity induced by microcystin-RR and microcystin-YR in differentiated and undifferentiated Caco-2 cells. Toxicon 54 (2): 161-169. doi:10.1016/j.toxicon.2009.03.030
  • Sancho E, Villarroel MJ, Ferrando MD (2016). Assessment of chronic effects of tebuconazole on survival, reproduction and growth of Daphnia magna after different exposure times. Ecotoxicology and Environmental Safety 124: 10-17. doi:10.1016/j.ecoenv.2015.09.034
  • Schmidt JR, Wilhelm SW, Boyer GL (2014). The fate of microcystins in the environment and challenges for monitoring. Toxins (Basel) 6 (12): 3354-87. doi:10.3390/toxins6123354
  • Sivonen K (1996). Cyanobacterial toxins and toxin production. Phycologia 35 (6S): 12-24. doi:10.2216/i0031-8884-35-6S-12.1
  • Smutná M, Babica P, Jarque S, Hilscherová KL, Maršálek B, Haeba M, Bláha L (2014). Acute, chronic and reproductive toxicity of complex cyanobacterial blooms in Daphnia magna and the role of microcystins. Toxicon 79: 11-18. doi:10.1016/j. toxicon.2013.12.009
  • Toporowska M, Mazur-Marzec H, Pawlik-Skowrońska B (2020). The effects of cyanobacterial bloom extracts on the biomass, Chl-a, MC and other Oligopeptides contents in a natural Planktothrixagardhii population. International Journal of Environmental Research and Public Health 17 (8), pii: E2881. doi:10.3390/ijerph17082881
  • Van Leeuwen CJ, Luttmer WJ, Griffieon PS (1985). The use of cohorts and populations in chronic toxicity studies with Daphnia magna: a cadmium example. Ecotoxicology and Environmental Safety 9 (1): 26-39. doi:10.1016/0147-6513(85)90031-4
  • Villarroel MJ, Sancho E, Ferrando MD, Andreu E (2003). Acute, chronic and sublethal effects of the herbicide propanil on Daphnia magna. Chemosphere 53 (8): 857-864. doi:10.1016/ S0045-6535(03)00546-0
  • Wiegand C (2009). Proteomic changes in Daphnia magna due to cyanobacterial toxins. In: SETAC Europe 19th, Protecting ecosystem health: facing the challenge of a globally changing environment; Göteborg, Sweden