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Journal of Toxicology
Volume 2011 (2011), Article ID 280304, 9 pages
http://dx.doi.org/10.1155/2011/280304
Research Article

Acute Exposure to Microcystin-Producing Cyanobacterium Microcystis aeruginosa Alters Adult Zebrafish (Danio rerio) Swimming Performance Parameters

1Laboratório de Biologia Genômica e Molecular, Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga 6681, 90619-900 Porto Alegre, RS, Brazil
2Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Hospital de Clínicas, Rua Ramiro Barcelos 2350, 90035-003 Porto Alegre, RS, Brazil
3Laboratório de Neuroquímica e Psicofarmacologia, Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga 6681, 90619-900 Porto Alegre, RS, Brazil
4Programa de Pós-Graduação em Farmacologia, Centro de Ciências da Saúde, Universidade Federal de Santa Maria, Avenida Roraima 1000, 97105-900 Santa Maria, RS, Brazil
5Curso de Medicina Veterinária, Universidade de Passo Fundo, Campus Universitário, Caixa Postal 611, 99001-970 Passo Fundo, RS, Brazil
6Unidade de Pesquisas em Cianobactérias, Prédio da Hidroquímica, Instituto de Oceanografia, Campus Carreiros da FURG, Caixa Postal 474, Rio Grande, RS, Brazil

Received 12 August 2011; Revised 15 September 2011; Accepted 22 September 2011

Academic Editor: J. J. Stegeman

Copyright © 2011 Luiza Wilges Kist et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. W. Carmichael, “Cyanobacteria secondary metabolites—the cyanotoxins,” Journal of Applied Bacteriology, vol. 72, no. 6, pp. 445–459, 1992. View at Google Scholar · View at Scopus
  2. R. M. Dawson, “The toxicology of microcystins,” Toxicon, vol. 36, no. 7, pp. 953–962, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Malbrouck and P. Kestemont, “Effects of microcystins on fish,” Environmental Toxicology and Chemistry, vol. 25, no. 1, pp. 72–86, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. M. F. Watanabe, K. I. Harada, W. W. Carmichael, and H. Fujiki, Toxic Microcystis, CRC Press, Boca Raton, Fla, USA, 1996.
  5. K. L. Rinehart, M. Namikoshi, and B. W. Choi, “Structure and biosynthesis of toxins from blue-green algae (cyanobacteria),” Journal of Applied Phycology, vol. 6, no. 2, pp. 159–176, 1994. View at Publisher · View at Google Scholar · View at Scopus
  6. K. D. Kearns and M. D. Hunter, “Toxin-producing Anabaena flos-aquae induces settling of Chlamydomonas reinhardtii, a competing motile alga,” Microbial Ecology, vol. 42, no. 1, pp. 80–86, 2001. View at Google Scholar · View at Scopus
  7. B. Puschner, F. D. Galey, B. Johnson et al., “Blue-green algae toxicosis in cattle,” Journal of the American Veterinary Medical Association, vol. 213, no. 11, pp. 1605–1607, 1998. View at Google Scholar · View at Scopus
  8. Y. Ueno, S. Nagata, T. Tsutsumi et al., “Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay,” Carcinogenesis, vol. 17, no. 6, pp. 1317–1321, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. W. W. Carmichael, S. M. Azevedo, J. S. An et al., “Human fatalities form cyanobacteria: chemical and biological evidence for cyanotoxins,” Environmental Health Perspectives, vol. 109, no. 7, pp. 663–668, 2001. View at Google Scholar · View at Scopus
  10. J. Chen, P. Xie, L. Li, and J. Xu, “First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage,” Toxicological Sciences, vol. 108, no. 1, pp. 81–89, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. P. F. Solter, G. K. Wollenberg, X. Huang, F. S. Chu, and M. T. Runnegar, “Prolonged sublethal exposure to protein phosphatase inhibitor microcystin-LR results in multiple dose-dependent hepatotoxic effects,” Toxicological Sciences, vol. 44, no. 1, pp. 87–96, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. L. Li, P. Xie, and J. Chen, “In vivo studies on toxin accumulation in liver and ultrastructural changes of hepatocytes of the phytoplanktivorous bighead carp i.p.-injected with extracted microcystins,” Toxicon, vol. 46, no. 5, pp. 533–545, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. U. S. Gupta and S. Guha, “Microcystin toxicity in a freshwater fish, Heteropneustes fossilis (Bloch),” Current Science, vol. 91, no. 9, pp. 1261–1271, 2006. View at Google Scholar · View at Scopus
  14. J. Ángeles, S. Pichardo, A. I. Prieto et al., “Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed tilapia fish (Oreochromis sp.) under laboratory conditions,” Aquatic Toxicology, vol. 72, no. 3, pp. 261–271, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. B. G. Kotak, S. Semalulu, D. L. Fritz, E. E. Prepas, S. E. Hrudey, and R. W. Coppock, “Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss),” Toxicon, vol. 34, no. 5, pp. 517–525, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. W. J. Fischer and D. R. Dietrich, “Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio),” Toxicology and Applied Pharmacology, vol. 164, no. 1, pp. 73–81, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. N. R. Bury, F. B. Eddy, and G. A. Codd, “The effects of the cyanobacterium Microcystis aeruginosa, the cyanobacterial hepatotoxin microcystin-LR, and ammonia on growth rate and ionic regulation of brown trout,” Journal of Fish Biology, vol. 46, no. 6, pp. 1042–1054, 1995. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Zhao, S. Xie, X. Zhu, Y. Yang, L. Gan, and L. Song, “Effect of inclusion of blue-green algae meal on growth and accumulation of microcystins in gibel carp (Carassius auratus gibelio),” Journal of Applied Ichthyology, vol. 22, no. 1, pp. 72–78, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. X. S. Ding, X. Y. Li, H. Y. Duan, I. K. Chung, and J. A. Lee, “Toxic effects of Microcystis cell extracts on the reproductive system of male mice,” Toxicon, vol. 48, no. 8, pp. 973–979, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. V. Vajcova, S. Navrátil, and M. Palíková, “The effect of intraperitoneally applied pure microcystin LR on haematological, biochemical and morphological indices of silver carp (Hypophthalmichthys molitrix Val.),” Acta Veterinaria, vol. 67, no. 4, pp. 281–287, 1998. View at Google Scholar · View at Scopus
  21. C. Malbrouck, G. Trausch, P. Devos, and P. Kestemont, “Hepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus L,” Comparative Biochemistry and Physiology: C, vol. 135, no. 1, pp. 39–48, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. X. Zhang, P. Xie, D. Li, and Z. Shi, “Hematological and plasma biochemical responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins with the possible mechanisms of anemia,” Toxicon, vol. 49, no. 8, pp. 1150–1157, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. C. M. McDermott, C. W. Nho, W. Howard, and B. Holton, “The cyanobacterial toxin, microcystin-LR, can induce apoptosis in a variety of cell types,” Toxicon, vol. 36, no. 12, pp. 1981–1996, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Lindholm, P. Öhman, K. Kurki-Helasmo, B. Kincaid, and J. Meriluoto, “Toxic algae and fish mortality in a brackish-water lake in Aland, SW Finland,” Hydrobiologia, vol. 397, pp. 109–120, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Scherer, “Behavioral responses as indicators of environmental alterations, approaches, results, developments,” Journal of Applied Ichthyology, vol. 8, no. 1–4, pp. 122–131, 1992. View at Google Scholar
  26. E. A. Paul and H. A. Simonin, “Effects of Naled, synergized,and non-synergized resmethrin on the swimming performance of young trout,” Bulletin of Environmental Contamination and Toxicology, vol. 57, no. 3, pp. 495–502, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. H. A. Campbell, R. D. Handy, and D. W. Sims, “Increased metabolic cost of swimming and consequent alterations to circadian activity in rainbow trout (Oncorhynchus mykiss) exposed to dietary copper,” Canadian Journal of Fisheries and Aquatic Sciences, vol. 59, no. 5, pp. 768–777, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. M. L. Begout Anras and J. P. Lagardère, “Measuring cultured fish swimming behaviour: first results on rainbow trout using acoustic telemetry in tanks,” Aquaculture, vol. 240, no. 1–4, pp. 175–186, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. R. F. Oliveira, V. C. Almada, and A. V. M. Canario, “Social modulation of sex steroid concentrations in the urine of male cichlid fish Oreochromis mossambicus,” Hormones and Behavior, vol. 30, no. 1, pp. 2–12, 1996. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. W. M. Contreras-Sánchez, C. B. Schreck, M. S. Fitzpatrick, and C. B. Pereira, “Effects of stress on the reproductive performance of rainbow trout (Oncorhynchus mykiss),” Biology of Reproduction, vol. 58, no. 2, pp. 439–447, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. T. G. Pottinger and T. R. Carrick, “Stress responsiveness affects dominant-subordinate relationships in rainbow trout,” Hormones and Behavior, vol. 40, no. 3, pp. 419–427, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. K. A. Sloman, N. B. Metcalfe, A. C. Taylor, and K. M. Gilmour, “Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout,” Physiological and Biochemical Zoology, vol. 74, no. 3, pp. 383–389, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. Ø. Øverli, T. G. Pottinger, T. R. Carrick, E. Øverli, and S. Winberg, “Differences in behaviour between rainbow trout selected for high- and low-stress responsiveness,” Journal of Experimental Biology, vol. 205, no. 3, pp. 391–395, 2002. View at Google Scholar · View at Scopus
  34. D. Baganz, G. Staaks, and C. Steinberg, “Impact of the cyanobacteria toxin, microcystin-LR on behaviour of zebrafish, Danio rerio,” Water Research, vol. 32, no. 3, pp. 948–952, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Baganz, G. Staaks, S. Pflugmacher, and C. E. W. Steinberg, “Comparative study of microcystin-LR-induced behavioral changes of two fish species, Danio rerio and Leucaspius delineatus,” Environmental Toxicology, vol. 19, no. 6, pp. 564–570, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. J. Cazenave, M. L. Nores, M. Miceli, M. P. Díaz, D. A. Wunderlin, and M. A. Bistoni, “Changes in the swimming activity and the glutathione S-transferase activity of Jenynsia multidentata fed with microcystin-RR,” Water Research, vol. 42, no. 4-5, pp. 1299–1307, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. D. E. Williams, M. L. Kent, R. J. Andersen, H. Klix, and C. F. B. Holmes, “Tissue distribution and clearance of tritium-labeled dihydromicrocystin-LR epimers administered to Atlantic salmon via intraperitoneal injection,” Toxicon, vol. 33, no. 2, pp. 125–131, 1995. View at Publisher · View at Google Scholar · View at Scopus
  38. V. O. Sipiä, H. T. Kankaanpää, J. Flinkman, K. Lahti, and J. A. O. Meriluoto, “Time-dependent accumulation of cyanobacterial hepatotoxins in flounders (Platichthys flesus) and mussels (Mytilus edulis) from the Northern Baltic Sea,” Environmental Toxicology, vol. 16, no. 4, pp. 330–336, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. Z. A. Mohamed, W. W. Carmichael, and A. A. Hussein, “Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom,” Environmental Toxicology, vol. 18, no. 2, pp. 137–141, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. L. Xie, P. Xie, K. Ozawa, T. Honma, A. Yokoyama, and H. D. Park, “Dynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment,” Environmental Pollution, vol. 127, no. 3, pp. 431–439, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Xie, P. Xie, L. Guo, L. Li, Y. Miyabara, and H. D. Park, “Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China,” Environmental Toxicology, vol. 20, no. 3, pp. 293–300, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. C. R. Carbis, J. A. Simons, P. Grant, G. F. Mitchell, J. W. Anderson, and I. McCauley, “A study of feral carp, Cyprinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health,” Journal of Fish Diseases, vol. 20, no. 2, pp. 81–91, 1997. View at Google Scholar · View at Scopus
  43. J. Cazenave, D. A. Wunderlin, M. D. L. A. Bistoni et al., “Uptake, tissue distribution and accumulation of microcystin-RR in Corydoras paleatus, Jenynsia multidentata and Odontesthes bonariensis: a field and laboratory study,” Aquatic Toxicology, vol. 75, no. 2, pp. 178–190, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. N. R. Bury, A. D. Newlands, F. B. Eddy, and G. A. Codd, “In vivo and in vitro intestinal transport of 3H-microcystin-LR, a cyanobacterial toxin, in rainbow trout (Oncorhynchus mykiss),” Aquatic Toxicology, vol. 42, no. 2, pp. 139–148, 1998. View at Publisher · View at Google Scholar · View at Scopus
  45. V. F. Magalhães, R. Moraes Soares, and S. M. F. O. Azevedo, “Microcystin contamination in fish from the Jacarepaguá Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk,” Toxicon, vol. 39, no. 7, pp. 1077–1085, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. V. F. Magalhães, M. M. Marinho, P. Domingos et al., “Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ),” Toxicon, vol. 42, no. 3, pp. 289–295, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Sahin, F. G. Tencalla, D. R. Dietrich, and H. Naegeli, “Biliary excretion of biochemically active cyanobacteria (blue-green algae) hepatotoxins in fish,” Toxicology, vol. 106, no. 1–3, pp. 123–130, 1996. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Tencalla and D. Dietrich, “Biochemical characterization of microcystin toxicity in rainbow trout (Oncorhynchus mykiss),” Toxicon, vol. 35, no. 4, pp. 583–595, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. L. I. Zon and R. T. Peterson, “In vivo drug discovery in the zebrafish,” Nature Reviews Drug Discovery, vol. 4, no. 1, pp. 35–44, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. J. M. Spitsbergen and M. L. Kent, “The state of the art of the zebrafish model for toxicology and toxicologic pathology research—advantages and current limitations,” Toxicologic Pathology, vol. 31, pp. 62–87, 2003. View at Google Scholar · View at Scopus
  51. A. L. Rubinstein, “Zebrafish: from disease modeling to drug discovery,” Current Opinion in Drug Discovery and Development, vol. 6, no. 2, pp. 218–223, 2003. View at Google Scholar · View at Scopus
  52. K. Dooley and L. I. Zon, “Zebrafish: a model system for the study of human disease,” Current Opinion in Genetics and Development, vol. 10, no. 3, pp. 252–256, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. G. J. Lieschke and P. D. Currie, “Animal models of human disease: zebrafish swim into view,” Nature Reviews Genetics, vol. 8, no. 5, pp. 353–367, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. J. D. Best and W. K. Alderton, “Zebrafish: an In vivo model for the study of neurological diseases,” Neuropsychiatric Disease and Treatment, vol. 4, no. 3, pp. 567–576, 2008. View at Google Scholar · View at Scopus
  55. R. J. Egan, C. L. Bergner, P. C. Hart et al., “Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish,” Behavioural Brain Research, vol. 205, no. 1, pp. 38–44, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. J. Cachat, P. Canavello, M. Elegante et al., “Modeling withdrawal syndrome in zebrafish,” Behavioural Brain Research, vol. 208, no. 2, pp. 371–376, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. C. Maximino, T. M. de Brito, C. A. Dias, A. Gouveia, and S. Morato, “Scototaxis as anxietylike behavior in fish.,” Nature Protocols, vol. 5, no. 2, pp. 209–216, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. A. Stewart, F. Kadri, and J. DiLeo, “The developing utility of zebrafish in modeling neurobehavioral disorders,” International Journal of Comparative Psychology, vol. 23, pp. 104–121, 2010. View at Google Scholar
  59. K. Wong, M. Elegante, B. Bartels et al., “Analyzing habituation responses to novelty in zebrafish (Danio rerio),” Behavioural Brain Research, vol. 208, no. 2, pp. 450–457, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. J. Kaslin and P. Panula, “Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio),” Journal of Comparative Neurology, vol. 440, no. 4, pp. 342–377, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. J. T. Shin and M. C. Fishman, “From zebrafish to human: modular medical models,” Annual Review of Genomics and Human Genetics, vol. 3, pp. 311–340, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. J. P. Gabriel, R. Mahmood, A. Kyriakatos et al., “Serotonergic modulation of locomotion in zebrafish: endogenous release and synaptic mechanisms,” Journal of Neuroscience, vol. 29, no. 33, pp. 10387–10395, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. T. Mueller, P. Vernier, and M. F. Wullimann, “The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio,” Brain Research, vol. 1011, no. 2, pp. 156–169, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. P. Panula, V. Sallinen, M. Sundvik et al., “Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases,” Zebrafish, vol. 3, no. 2, pp. 235–247, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. R. Gerlai, V. Lee, and R. Blaser, “Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio),” Pharmacology Biochemistry and Behavior, vol. 85, no. 4, pp. 752–761, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. G. Li, J. Chen, P. Xie, Y. Jiang, L. Wu, and X. Zhang, “Protein expression profiling in the zebrafish (Danio rerio) embryos exposed to the microcystin-LR,” Proteomics, vol. 11, no. 10, pp. 2003–2018, 2011. View at Google Scholar
  67. Y. Zhao, Q. Xiong, and P. Xie, “Analysis of microRNA expression in embryonic developmental toxicity induced by MC-RR,” PLoS One, vol. 6, no. 7, Article ID e22676, 2011. View at Google Scholar
  68. P. J. Oberholster, J. G. Myburgh, D. Govender, R. Bengis, and A. M. Botha, “Identification of toxigenic Microcystis strains after incidents of wild animal mortalities in the Kruger National Park, South Africa,” Ecotoxicology and Environmental Safety, vol. 72, no. 4, pp. 1177–1182, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. L. C. Backer, S. V. McNeel, T. Barber et al., “Recreational exposure to microcystins during algal blooms in two California lakes,” Toxicon, vol. 55, no. 5, pp. 909–921, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. R. Gerlai, M. Lahav, S. Guo, and A. Rosenthal, “Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects,” Pharmacology Biochemistry and Behavior, vol. 67, no. 4, pp. 773–782, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. E. D. Levin, Z. Bencan, and D. T. Cerutti, “Anxiolytic effects of nicotine in zebrafish,” Physiology & Behavior, vol. 90, no. 1, pp. 54–58, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. R. Gerlai, “Zebra fish: an uncharted behavior genetic model,” Behavior Genetics, vol. 33, no. 5, pp. 461–468, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. A. L. Piato, D. B. Rosemberg, K. M. Capiotti et al., “Acute restraint stress in zebrafish: behavioral parameters and purinergic signaling,” Neurochemical Research, vol. 36, no. 10, pp. 1876–1886, 2011. View at Google Scholar
  74. L. J. G. Barcellos, F. Ritter, L. C. Kreutz et al., “Whole-body cortisol increases after direct and visual contact with a predator in zebrafish Danio rerio,” Aquaculture, vol. 272, no. 1–4, pp. 774–778, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Oberemm, J. Becker, G. A. Codd, and C. Steinberg, “Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians,” Environmental Toxicology, vol. 14, no. 1, pp. 77–88, 1999. View at Google Scholar · View at Scopus
  76. C. Pietsch, C. Wiegand, M. V. Amé, A. Nicklisch, D. Wunderlin, and S. Pflugmacher, “The effects of a cyanobacterial crude extract on different aquatic organisms: evidence for cyanobacterial toxin modulating factors,” Environmental Toxicology, vol. 16, no. 6, pp. 535–542, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. S. M. Zala and D. J. Penn, “Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges,” Animal Behaviour, vol. 68, no. 4, pp. 649–664, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. L. Saint-Amant and P. Drapeau, “Time course of the development of motor behaviors in the zebrafish embryo,” Journal of Neurobiology, vol. 37, no. 4, pp. 622–632, 1998. View at Google Scholar · View at Scopus
  79. L. Saint-Amant and P. Drapeau, “Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling,” Neuron, vol. 31, no. 6, pp. 1035–1046, 2001. View at Publisher · View at Google Scholar · View at Scopus
  80. M. A. Borla, B. Palecek, S. Budick, and D. M. O'Malley, “Prey capture by larval zebrafish: evidence for fine axial motor control,” Brain, Behavior and Evolution, vol. 60, no. 4, pp. 207–229, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Watkins, A. Miklosi, and R. J. Andrew, “Early asymmetries in the behaviour of zebrafish larvae,” Behavioural Brain Research, vol. 151, no. 1-2, pp. 177–183, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. E. Loucks and M. J. Carvan, “Strain-dependent effects of developmental ethanol exposure in zebrafish,” Neurotoxicology and Teratology, vol. 26, no. 6, pp. 745–755, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  83. S. Damodaran, C. A. Dlugos, T. D. Wood, and R. A. Rabin, “Effects of chronic ethanol administration on brain protein levels: a proteomic investigation using 2-D DIGE system,” European Journal of Pharmacology, vol. 547, no. 1–3, pp. 75–82, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. M. J. Airhart, D. H. Lee, T. D. Wilson, B. E. Miller, M. N. Miller, and R. G. Skalko, “Movement disorders and neurochemical changes in zebrafish larvae after bath exposure to fluoxetine (PROZAC),” Neurotoxicology and Teratology, vol. 29, no. 6, pp. 652–664, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. M. Pyron, “Female preferences and male-male interactions in zebrafish (Danio rerio),” Canadian Journal of Zoology, vol. 81, no. 1, pp. 122–125, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. R. E. Engeszer, M. J. Ryan, and D. M. Parichy, “Learned social preference in zebrafish,” Current Biology, vol. 14, no. 10, pp. 881–884, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. S. L. S. Bass and R. Gerlai, “Zebrafish (Danio rerio) responds differentially to stimulus fish: the effects of sympatric and allopatric predators and harmless fish,” Behavioural Brain Research, vol. 186, no. 1, pp. 107–117, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. K. D. Mann, E. R. Turnell, J. Atema, and G. Gerlach, “Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues,” The Biological Bulletin, vol. 205, no. 2, pp. 224–225, 2003. View at Google Scholar · View at Scopus
  89. A. Vitebsky, R. Reyes, M. J. Sanderson, W. C. Michel, and K. E. Whitlock, “Isolation and characterization of the laure olfactory behavioral mutant in the zebrafish, Danio rerio,” Developmental Dynamics, vol. 234, no. 1, pp. 229–242, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. T. Darland and J. E. Dowling, “Behavioral screening for cocaine sensitivity in mutagenized zebrafish,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 20, pp. 11691–11696, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. J. Ninkovic and L. Bally-Cuif, “The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse,” Methods, vol. 39, no. 3, pp. 262–274, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. L. J. Kily, Y. C. Cowe, O. Hussain et al., “Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways,” Journal of Experimental Biology, vol. 211, no. 10, pp. 1623–1634, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  93. C. Cirelli and G. Tononi, “Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system,” Journal of Neuroscience, vol. 20, no. 24, pp. 9187–9194, 2000. View at Google Scholar · View at Scopus
  94. F. E. Williams, D. White, and W. S. Messer, “A simple spatial alternation task for assessing memory function in zebrafish,” Behavioural Processes, vol. 58, no. 3, pp. 125–132, 2002. View at Publisher · View at Google Scholar · View at Scopus
  95. R. M. Colwill, M. P. Raymond, L. Ferreira, and H. Escudero, “Visual discrimination learning in zebrafish (Danio rerio),” Behavioural Processes, vol. 70, no. 1, pp. 19–31, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  96. I. Plaut, “Effects of fin size on swimming performance, swimming behaviour and routine activity of zebrafish Danio rerio,” Journal of Experimental Biology, vol. 203, no. 4, pp. 813–820, 2000. View at Google Scholar · View at Scopus
  97. R. Blaser and R. Gerlai, “Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods,” Behavior Research Methods, vol. 38, no. 3, pp. 456–469, 2006. View at Google Scholar · View at Scopus
  98. R. Spence, G. Gerlach, C. Lawrence, and C. Smith, “The behavior and ecology of the zebrafish, Danio rerio,” Biological Reviews of the Cambridge Philosofical Society, vol. 83, no. 1, pp. 13–34, 2008. View at Google Scholar
  99. A. J. W. Ward, A. J. Duff, and S. Currie, “The effects of the endocrine disrupter 4-nonylphenol on the behaviour of juvenile rainbow trout (Oncorhynchus mykiss),” Canadian Journal of Fisheries and Aquatic Sciences, vol. 63, no. 2, pp. 377–382, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. P. Saglio and S. Trijasse, “Behavioral responses to atrazine and diuron in goldfish,” Archives of Environmental Contamination and Toxicology, vol. 35, no. 3, pp. 484–491, 1998. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Xia, C. Niu, and X. Pei, “Effects of chronic exposure to nonylphenol on locomotor activity and social behavior in zebrafish (Danio rerio),” Journal of Environmental Sciences, vol. 22, no. 9, pp. 1435–1440, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. B. A. Barton, “Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids,” Integrative and Comparative Biology, vol. 42, no. 3, pp. 517–525, 2002. View at Google Scholar · View at Scopus
  103. A. L. Piato, K. M. Capiotti, A. R. Tamborski et al., “Unpredictable chronic stress model in zebrafish (Danio rerio): behavioral and physiological responses,” Progress in Neuro-Psychopharmacology & Biological Psychiatry, vol. 35, no. 2, pp. 561–567, 2011. View at Google Scholar
  104. N. R. Bury, F. B. Eddy, and G. A. Codd, “The stress responses of brown trout, Salmo truffa L, to the cyanobacterium, Microcystis aeruginosa,” Environmental Toxicology and Water Quality, vol. 11, no. 3, pp. 187–193, 1996. View at Google Scholar · View at Scopus
  105. D. Li, P. Xie, and X. Zhang, “Changes in plasma thyroid hormones and cortisol levels in crucian carp (Carassius auratus) exposed to the extracted microcystins,” Chemosphere, vol. 74, no. 1, pp. 13–18, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus