Effects of phytoplankton extracts containing the toxin microcystin-LR on the survival and reproduction of cladocerans

Toxicon

Volumn 95, Issue , 2015, Pages 38-45

  Herrera, Natalia A ^a   Echeverri, Luis Fernando ^a   Ferrão Filho, Aloysio S ^b  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Acute effect; Chronic effect; Cladocerans; Cyanobacterial extracts; Microcystins

Indexed keywords

ALGAL EXTRACT; MICROCYSTIN LR; PHYTOPLANKTON EXTRACT; UNCLASSIFIED DRUG; MARINE TOXIN; MICROCYSTIN;

ACUTE TOXICITY; ARTICLE; BODY GROWTH; CHRONIC TOXICITY; CLADOCERA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DAPHNIA; DAPHNIA SIMILIS; EGG PRODUCTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LC50; MASS SPECTROMETRY; MICROCYSTIS; MOINA MICRURA; NONHUMAN; PHYTOPLANKTON; REPRODUCTION; SURVIVAL; TOXICITY TESTING; TOXIN ANALYSIS; ANIMAL; CHEMISTRY; CYANOBACTERIUM; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; LD50; MICROBIOLOGY; TANDEM MASS SPECTROMETRY;

CYANOBACTERIA; DAPHNIA; DAPHNIA LAEVIS; DAPHNIA SIMILIS; MICROCYSTIS; MOINA MICRURA;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLADOCERA; CYANOBACTERIA; DAPHNIA; LETHAL DOSE 50; MARINE TOXINS; MICROCYSTINS; PHYTOPLANKTON; REPRODUCTION; TANDEM MASS SPECTROMETRY; TOXICITY TESTS, ACUTE; TOXICITY TESTS, CHRONIC;

EID: 84920720976     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2014.12.016     Document Type: Article

References (57)

1. ABNT. Associação Brasileira de Normas Técnicas-NBR 12713. Ecotoxicologia aquática - Toxicidade aguda - Método de ensaio com Daphnia spp. (Cladocera, crustacea) 2004 ABNT Rio de Janeiro
2. M. Agrawal, D. Bagchi, and S. Bagchi Acute inhibition of protease and suppression of growth in zooplankter, Moina macrocopa, by Microcystis blooms collected in Central India Hydrobiologia 464 1-3 2001 37 44
3. M.K. Agrawal, A. Zitt, D. Bagchi, J. Weckesser, S.N. Bagchi, and E. von Elert Characterization of proteases in guts of Daphnia magna and their inhibition by Microcystis aeruginosa PCC 7806 Environ. Toxicol. 20 3 2005 314 322
4. S.M.F.O. Azevedo, W.W. Carmichael, E.M. Jochimsen, K.L. Rinehart, S. Lau, G.R. Shaw, and G.K. Eaglesham Human intoxication by microcystins during renal dialysis treatment in Caruaru - Brazil Toxicology 181 2002 441 446
5. W.W. Carmichael Cyanobacteria secondary metabolites-the cyanotoxins J. Appl. Microbiol. 72 6 1992 445 459
6. W.W. Carmichael The toxins of cyanobacteria Sci. Am. 270 1 1994 78 86
7. G.A. Codd, J.S. Metcalf, and K.A. Beattie Retention of Microcystis aeruginosa and microcystin by salad lettuce (Lactuca sativa) after spray irrigation with water containing cyanobacteria Toxicon 37 8 1999 1181 1185
8. W. Chen, L. Song, D. Ou, and N. Gan Chronic toxicity and responses of several important enzymes in Daphnia magna on exposure to sublethal microcystin-LR Environ. Toxicol. 20 3 2005 323 330
9. T.S. Dao, L.C. Do-Hong, and C. Wiegand Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring Toxicon 55 7 2010 1244 1254
10. W.R. DeMott, and S. Dhawale Inhibition of in vitro protein phosphatase activity in three zooplâncton species by microcystin-LR, a toxin from cyanobacteria Arch. Hydorbiol. 134 4 1995 417 424
11. W.R. DeMott, and F. Moxter Foraging cyanobacteria by copepods: responses to chemical defense and resource abundance Ecology 72 1991 1820 1834
12. W.R. DeMott, Q.X. Zhang, and W.W. Carmichael Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia Limnol. Oceanogr. 36 7 1991 1346 1357
13. F.A. Dörr, E. Pinto, R.M. Soares, and S.M. Feliciano de Oliveira e Azevedo Microcystins in South American aquatic ecosystems: occurrence, toxicity and toxicological assays Toxicon 56 7 2010 1247 1256
14. C. Edwards, D. Graham, N. Fowler, and L.A. Lawton Biodegradation of microcystins and nodularin in freshwaters Chemosphere 73 8 2008 1315 1321
15. A. Escobar, and G. Manjarrés Estudio de un florecimiento de algas tóxicas en la Ciénaga San Rafael de Buenavista, Magdalena-Colombia 1985 Universidad Tecnológica del Magdalena. Facultad de Ciencias de la Educación Santa Marta. Colombia
16. A. Ferrão-Filho, and S.O. Azevedo Effects of unicellular and colonial forms of toxic Microcystis aeruginosa from laboratory cultures and natural populations on tropical cladocerans Aquat. Toxicol. 37 1 2003 23 35
17. A.D.S. Ferrão-Filho, and B. Kozlowsky-Suzuki Cyanotoxins: bioaccumulation and effects on aquatic animals Mar. Drugs 9 12 2011 2729 2772
18. A.D.S. Ferrão-Filho, M.C.S. Soares, V. De Freitas Magalhães, and S.M.F.O. Azevedo Biomonitoring of cyanotoxins in two tropical reservoirs by cladoceran toxicity bioassays Ecotoxicol. Environ. Saf. 72 2 2009 479 489
19. A.S. FerrÃo-Filho, S.M.F.O. Azevedo, and W.R. DeMott Effects of toxic and non-toxic cyanobacteria on the life history of tropical and temperate cladocerans Freshw. Biol. 45 1 2000 1 19
20. A.S. Ferrão-Filho, S.M. da Costa, M.G.L. Ribeiro, and S.M.F.O. Azevedo Effects of a saxitoxin-producer strain of Cylindrospermopsis raciborskii (cyanobacteria) on the swimming movements of cladocerans Environ. Toxicol. 23 2 2008 161 168
21. A.S. Ferrão-Filho, N.A. Herrera, and L.F. Echeverri Microcystin accumulation in cladocerans: first evidence of MC uptake from aqueous extracts of a natural bloom sample Toxicon 87 2014 26 31
22. J.E. Galeano, and J.A. Villalobos Cianobacterias y Microcistinas en el Caribe Colombiano: Identificación de cianobacterias y detección de microcistinas en el antiguo delta del río Sinú Córdoba - Colombia 2010
23. A. Ghadouani, B. Pinel-Alloul, K. Plath, G.A. Codd, and W. Lampert Effects of Microcystis aeruginosa and purified microcystin-LR on the feeding behavior of Daphnia pulicaria Limnol. Oceanogr. 49 3 2004 666 679
24. N. Gupta, S.C. Pant, R. Vijayaraghavan, and P.V.L. Rao Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice Toxicology 188 2 2003 285 296
25. S. Gustafsson, K. Rengefors, and L.A. Hansson Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects Ecology 86 10 2005 2561 2567
26. R.E. Guzman, P.F. Solter, and M.T. Runnegar Inhibition of nuclear protein phosphatase activity in mouse hepatocytes by the cyanobacterial toxin microcystin-LR Toxicon 41 7 2003 773 781
27. N.G. Hairston, C.L. Holtmeier, W. Lampert, L.J. Weider, D.M. Post, J.M. Fischer, C.E. Cáceres, J.A. Fox, and U. Gaedke Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55 11 2001 2203 2214
28. K.I. Harada, M. Oshikata, H. Uchida, M. Suzuki, F. Kondo, K. Sato, Y. Ueno, S.Z. Yu, G. Chen, and G.C. Chen Detection and identification of microcystins in the drinking water of Haimen City, China Nat. Toxins 4 6 1996 277 283
29. J. Hietala, C. Laurén-Määttä, and M. Walls Sensitivity of Daphnia to toxic cyanobacteria: effects of genotype and temperature Freshw. Biol. 37 2 1997 299 306
30. J. Hietala, M. Reinikainen, and M. Walls Variation in life history responses of Daphnia to toxic Microcystis aeruginosa J. Plankton Res. 17 12 1995 2307 2318
31. C. Jakobi, K.L. Rinehart, R. Neuber, K. Mez, and J. Weckesser Cyanopeptolin SS, a disulphated depsipeptide from a water bloom: structural elucidation and biological activities Phycologia 35 6S 1996 111 116
32. D. Jungmann Isolation, purification, and characterization of new daphnia-toxic compound from axenic Microcystis flos-aquae strain PCC7806 J. Chem. Ecol. 21 11 1995 1665 1676
33. D. Jungmann, and J. Benndorf Toxicity to Daphnia of a compound extracted from laboratory and natural Microcystis spp., and the role of microcystins Freshw. Biol. 32 1 1994 13 20
34. C. Laurén-Määttä, J. Hietala, and M. Andwalls Responses of Daphnia pulex populations to toxic cyanobacteria Freshw. Biol. 37 3 1997 635 647
35. H. Li, T. Murphy, J. Guo, T. Parr, and C. Nalewajko Iron-stimulated growth and microcystin production of Microcystis novacekii UAM 250 Limnologica 39 3 2009 255 259
36. M. Lürling Effects of microcystin-free and microcystin-containing strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna Environ. Toxicol. 18 3 2003 202 210
37. P. Mancera, J.E., and V.L.A. Vidal Florecimiento de microalgas relacionado con mortandad masiva de peces en el complejo lagunar ciénaga grande de santa marta, caribe colombiano Bol. Investig. Mar. Costeras - Invemar 23 1994 103 117
38. J. McElhiney, and L.A. Lawton Detection of the cyanobacterial hepatotoxins microcystins Toxicol. Appl. Pharmacol. 203 3 2005 219 230
39. J. Meriluoto, L. Lawton, and K.I. Harada O. Holst, Isolation and Detection of Microcystins and Nodularins, Cyanobacterial Peptide Hepatotoxins. Bacterial Toxins: Methods and Protocols vol. 145 2000 Humana Press 65 87
40. N.J.C. Monteiro, J. Yunes, and M.B. Bohrer-Morel Effects of the Microcystis aeruginosa strain rsT9501 from Patos lagoon, rs, on the growth and reproduction of the cladoceran Ceriodaphnia dubia JBSE 1 2006 93 96
41. D. Okumura, R. Sotero-Santos, R. Takenaka, and O. Rocha Evaluation of cyanobacteria toxicity in tropical reservoirs using crude extracts bioassay with cladocerans Ecotoxicology 16 2 2007 263 270
42. J. Osswald, S. Rellán, A. Gago, and V. Vasconcelos Uptake and depuration of anatoxin-a by the mussel Mytilus galloprovincialis (Lamarck, 1819) under laboratory conditions Chemosphere 72 9 2008 1235 1241
43. M. Reinikainen, J. Hietala, and M. Walls Adaptations and resistance of zooplankton to stress: effects of genetic, environmental, and physiological factors Ecotoxicol. Environ. Saf. 40 1 1998 77 80
44. M. Rivera Gonzalez, and L. Gómez Gómez Identificación de cianobacterias potencialmente productoras de cianotoxinas en la curva de salguero del río Cesar Rev. Luna Azul 31 2010 17 25
45. T. Rohrlack, K. Christoffersen, E. Dittmann, I. Nogueira, V. Vasconcelos, and T. Börner Ingestion of microcystins by Daphnia: intestinal uptake and toxic effects Limnol. Oceanogr. 50 2005 440 448
46. J. Ros Prácticas de Ecología 1979 Ediciones Omega SA, Barcelona 181
47. L.N. Sangolkar, S.S. Maske, and T. Chakrabarti Methods for determining microcystins (peptide hepatotoxins) and microcystin-producing cyanobacteria Water Res. 40 19 2006 3485 3496
48. M. Smutná, P. Babica, S. Jarque, K. Hilscherová, B. Marsálek, M. Haeba, and L. Bláha Acute, chronic and reproductive toxicity of complex cyanobacterial blooms in Daphnia magna and the role of microcystins Toxicon 79 2014 11 18
49. I.L. Trubetskova, and J.F. Haney Effects of differing concentrations of microcystin-producing Microcystis aeruginosa on growth, reproduction, survivorship and offspring of Daphnia magna Arch. Hydrobiol. 167 1-4 2006 533 546
50. M.E. Van Apeldoorn, H.P. Van Egmond, G.J.A. Speijers, and G.J.I. Bakker Toxins of cyanobacteria Mol. Nutr. Food Res. 51 1 2007 7 60
51. C. Wiegand, and S. Pflugmacher Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review Toxicol. Appl. Pharmacol. 203 3 2005 201 218
52. A.E. Wilson, and M.E. Hay A direct test of cyanobacterial chemical defense: variable effects of microcystin-treated food on two Daphnia pulicaria clones Limnol. Oceanogr. 52 4 2007 1467
53. M. Yasuno, and Y. Sugaya Toxicities of Microcystis viridis and the isolated hepatotoxic polypeptides on cladocerans Verh. Int. Ver. Limnol. 24 4 1991 2622 2626
54. M. Yasuno, Y. Sugaya, K. Kaya, and M.M. Watanabe Variations in the toxicity of Microcystis species to Moina macrocopa Phycol. Res. 46 s2 1998 31 36
55. A. Zaccaroni, and D. Scaravelli V. Evangelista, L. Barsanti, A. Frassanito, V. Passarelli, P. Gualtieri, Toxicity of Fresh Water Algal Toxins to Humans and Animals. Algal Toxins: Nature, Occurrence, Effect and Detection 2008 Springer Netherlands 45 89
56. A. Zaccaroni, and D. Scaravelli V. Evangelista, L. Barsanti, A. Frassanito, V. Passarelli, P. Gualtieri, Toxicity of sea Algal Toxins to Humans and Animals. Algal Toxins: Nature, Occurrence, Effect and Detection 2008 Springer Netherlands 91 158
57. B. Žegura, T.T. Lah, and M. Filipič Alteration of intracellular GSH levels and its role in microcystin-LR-induced DNA damage in human hepatoma HepG2 cells Mutat. Res. Gen. Toxicol. Environ. 611 1 2006 25 33