Acute exposure to microcystin-producing cyanobacterium microcystis aeruginosa alters adult zebrafish (Danio rerio) swimming performance parameters

Journal of Toxicology

Volumn 2011, Issue , 2011, Pages

  Kist, Luiza Wilges ^a,b   Piato, Angelo Luis ^a,b   Da Rosa, João Gabriel Santos ^c   Koakoski, Gessi ^c   Barcellos, Leonardo José Gil ^d   Yunes, João Sarkis ^e   Bonan, Carla Denise ^a,b   Bogo, Maurício Reis ^a,b  

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b Hospital de Clnicas   (Brazil)

^c FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^d UNIVERSITY OF PASSO FUNDO   (Brazil)

^e FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROCORTISONE; MICROCYSTIN;

ARTICLE; CONTROLLED STUDY; EXPOSURE; IMMOBILIZATION; MICROCYSTIS AERUGINOSA; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SWIMMING; ZEBRA FISH;

ALGAE; ANIMALIA; CHLOROPHYTA; CYANOBACTERIA; DANIO RERIO; MICROCYSTIS AERUGINOSA;

EID: 84855611603     PISSN: 16878191     EISSN: 16878205     Source Type: Journal    
DOI: 10.1155/2011/280304     Document Type: Article

References (105)

1. Carmichael W. W., Cyanobacteria secondary metabolitesthe cyanotoxins Journal of Applied Bacteriology 1992 72 6 445 459
2. Dawson R. M., The toxicology of microcystins Toxicon 1998 36 7 953 962 (Pubitemid 28305389)
3. Malbrouck C., Kestemont P., Effects of microcystins on fish Environmental Toxicology and Chemistry 2006 25 1 72 86 (Pubitemid 43031204)
4. Watanabe M. F., Harada K. I., Carmichael W. W., Fujiki H., Toxic Microcystis 1996 Boca Raton, Fla, USA CRC Press
5. Rinehart K. L., Namikoshi M., Choi B. W., Structure and biosynthesis of toxins from blue-green algae (cyanobacteria) Journal of Applied Phycology 1994 6 2 159 176
6. Kearns K. D., Hunter M. D., Toxin-producing Anabaena flos-aquae induces settling of Chlamydomonas reinhardtii, a competing motile alga Microbial Ecology 2001 42 1 80 86 (Pubitemid 32731573)
7. Puschner B., Galey F. D., Johnson B., Dickie C. W., Vondy M., Francis T., Holstege D. M., Blue-green algae toxicosis in cattle Journal of the American Veterinary Medical Association 1998 213 11 1605 1607 (Pubitemid 128472511)
8. Ueno Y., Nagata S., Tsutsumi T., Hasegawa A., Watanabe M. F., Park H. D., Chen G. C., Chen G., Yu S. Z., 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 1996 17 6 1317 1321 (Pubitemid 26196344)
9. Carmichael W. W., Azevedo S. M., An J. S., Molica R. J. R., Jochimsen E. M., Lau S., Rinehart K. L., Shaw G. R., Eaglesham G. K., Human fatalities form cyanobacteria: chemical and biological evidence for cyanotoxins Environmental Health Perspectives 2001 109 7 663 668 (Pubitemid 32785421)
10. Chen J., Xie P., Li L., Xu J., First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage Toxicological Sciences 2009 108 1 81 89
11. Solter P. F., Wollenberg G. K., Huang X., Chu F. S., Runnegar M. T., Prolonged sublethal exposure to protein phosphatase inhibitor microcystin-LR results in multiple dose-dependent hepatotoxic effects Toxicological Sciences 1998 44 1 87 96 (Pubitemid 28378053)
12. Li L., Xie P., Chen J., 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 2005 46 5 533 545 (Pubitemid 41253371)
13. Gupta U. S., Guha S., Microcystin toxicity in a freshwater fish, Heteropneustes fossilis (Bloch) Current Science 2006 91 9 1261 1271 (Pubitemid 44846627)
14. ngeles J., Pichardo S., Prieto A. I., Repetto G., Vzquez C. M., Moreno I., Camen A. M., Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed tilapia fish (Oreochromis sp.) under laboratory conditions Aquatic Toxicology 2005 72 3 261 271 (Pubitemid 40487515)
15. Kotak B. G., Semalulu S., Fritz D. L., Prepas E. E., Hrudey S. E., Coppock R. W., Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss) Toxicon 1996 34 5 517 525 (Pubitemid 26164340)
16. Fischer W. J., Dietrich D. R., Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio) Toxicology and Applied Pharmacology 2000 164 1 73 81 (Pubitemid 30198546)
17. Bury N. R., Eddy F. B., Codd G. A., 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 1995 46 6 1042 1054
18. Zhao M., Xie S., Zhu X., Yang Y., Gan L., Song L., Effect of inclusion of blue-green algae meal on growth and accumulation of microcystins in gibel carp (Carassius auratus gibelio) Journal of Applied Ichthyology 2006 22 1 72 78 (Pubitemid 43733183)
19. Ding X. S., Li X. Y., Duan H. Y., Chung I. K., Lee J. A., Toxic effects of Microcystis cell extracts on the reproductive system of male mice Toxicon 2006 48 8 973 979
20. Vajcova V., Navrtil S., Palkov M., The effect of intraperitoneally applied pure microcystin LR on haematological, biochemical and morphological indices of silver carp (Hypophthalmichthys molitrix Val.) Acta Veterinaria 1998 67 4 281 287 (Pubitemid 128537883)
21. Malbrouck C., Trausch G., Devos P., Kestemont P., Hepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus L Comparative Biochemistry and Physiology: C 2003 135 1 39 48 (Pubitemid 36644990)
22. Zhang X., Xie P., Li D., Shi Z., Hematological and plasma biochemical responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins with the possible mechanisms of anemia Toxicon 2007 49 8 1150 1157 (Pubitemid 46813149)
23. McDermott C. M., Nho C. W., Howard W., Holton B., The cyanobacterial toxin, microcystin-LR, can induce apoptosis in a variety of cell types Toxicon 1998 36 12 1981 1996 (Pubitemid 28532776)
24. Lindholm T., hman P., Kurki-Helasmo K., Kincaid B., Meriluoto J., Toxic algae and fish mortality in a brackish-water lake in Aland, SW Finland Hydrobiologia 1999 397 109 120 (Pubitemid 29475323)
25. Scherer E., Behavioral responses as indicators of environmental alterations, approaches, results, developments Journal of Applied Ichthyology 1992 8 14 122 131
26. Paul E. A., Simonin H. A., Effects of Naled, synergized,and non-synergized resmethrin on the swimming performance of young trout Bulletin of Environmental Contamination and Toxicology 1996 57 3 495 502
27. Campbell H. A., Handy R. D., Sims D. W., 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 2002 59 5 768 777
28. Begout Anras M. L., Lagardre J. P., Measuring cultured fish swimming behaviour: first results on rainbow trout using acoustic telemetry in tanks Aquaculture 2004 240 14 175 186
29. Oliveira R. F., Almada V. C., Canario A. V. M., Social modulation of sex steroid concentrations in the urine of male cichlid fish Oreochromis mossambicus Hormones and Behavior 1996 30 1 2 12 (Pubitemid 26179506)
30. Contreras-Snchez W. M., Schreck C. B., Fitzpatrick M. S., Pereira C. B., Effects of stress on the reproductive performance of rainbow trout (Oncorhynchus mykiss) Biology of Reproduction 1998 58 2 439 447 (Pubitemid 28099110)
31. Pottinger T. G., Carrick T. R., Stress responsiveness affects dominant-subordinate relationships in rainbow trout Hormones and Behavior 2001 40 3 419 427 (Pubitemid 33063570)
32. Sloman K. A., Metcalfe N. B., Taylor A. C., Gilmour K. M., Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout Physiological and Biochemical Zoology 2001 74 3 383 389 (Pubitemid 32501225)
33. verli., Pottinger T. G., Carrick T. R., verli E., Winberg S., Differences in behaviour between rainbow trout selected for high- and low-stress responsiveness Journal of Experimental Biology 2002 205 3 391 395 (Pubitemid 34853803)
34. Baganz D., Staaks G., Steinberg C., Impact of the cyanobacteria toxin, microcystin-LR on behaviour of zebrafish, Danio rerio Water Research 1998 32 3 948 952 (Pubitemid 28075242)
35. Baganz D., Staaks G., Pflugmacher S., Steinberg C. E. W., Comparative study of microcystin-LR-induced behavioral changes of two fish species, Danio rerio and Leucaspius delineatus Environmental Toxicology 2004 19 6 564 570 (Pubitemid 39552266)
36. Cazenave J., Nores M. L., Miceli M., Daz M. P., Wunderlin D. A., Bistoni M. A., Changes in the swimming activity and the glutathione S-transferase activity of Jenynsia multidentata fed with microcystin-RR Water Research 2008 42 4-5 1299 1307 (Pubitemid 351231976)
37. Williams D. E., Kent M. L., Andersen R. J., Klix H., Holmes C. F. B., Tissue distribution and clearance of tritium-labeled dihydromicrocystin-LR epimers administered to Atlantic salmon via intraperitoneal injection Toxicon 1995 33 2 125 131
38. Sipi V. O., Kankaanp H. T., Flinkman J., Lahti K., Meriluoto J. A. O., Time-dependent accumulation of cyanobacterial hepatotoxins in flounders (Platichthys flesus) and mussels (Mytilus edulis) from the Northern Baltic Sea Environmental Toxicology 2001 16 4 330 336 (Pubitemid 32734206)
39. Mohamed Z. A., Carmichael W. W., Hussein A. A., Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom Environmental Toxicology 2003 18 2 137 141 (Pubitemid 44783331)
40. Xie L., Xie P., Ozawa K., Honma T., Yokoyama A., Park H. D., Dynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment Environmental Pollution 2004 127 3 431 439 (Pubitemid 37443644)
41. Xie L., Xie P., Guo L., Li L., Miyabara Y., Park H. D., Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China Environmental Toxicology 2005 20 3 293 300 (Pubitemid 40827448)
42. Carbis C. R., Simons J. A., Grant P., Mitchell G. F., Anderson J. W., McCauley I., 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 1997 20 2 81 91
43. Cazenave J., Wunderlin D. A., Bistoni M. D. L. A., Amé M. V., Krause E., Pflugmacher S., Wiegand C., Uptake, tissue distribution and accumulation of microcystin-RR in Corydoras paleatus, Jenynsia multidentata and Odontesthes bonariensis: a field and laboratory study Aquatic Toxicology 2005 75 2 178 190 (Pubitemid 41338588)
44. Bury N. R., Newlands A. D., Eddy F. B., Codd G. A., In vivo and in vitro intestinal transport of 3H-microcystin-LR, a cyanobacterial toxin, in rainbow trout (Oncorhynchus mykiss) Aquatic Toxicology 1998 42 2 139 148 (Pubitemid 28273072)
45. Magalhes V. F., Moraes Soares R., Azevedo S. M. F. O., Microcystin contamination in fish from the Jacarepagu Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk Toxicon 2001 39 7 1077 1085 (Pubitemid 32166959)
46. Magalhes V. F., Marinho M. M., Domingos P., Oliveira A. C., Costa S. M., Azevedo L. O., Azevedo S. M. F. O., Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ) Toxicon 2003 42 3 289 295 (Pubitemid 37338165)
47. Sahin A., Tencalla F. G., Dietrich D. R., Naegeli H., Biliary excretion of biochemically active cyanobacteria (blue-green algae) hepatotoxins in fish Toxicology 1996 106 13 123 130 (Pubitemid 26038281)
48. Tencalla F., Dietrich D., Biochemical characterization of microcystin toxicity in rainbow trout (Oncorhynchus mykiss) Toxicon 1997 35 4 583 595 (Pubitemid 27158354)
49. Zon L. I., Peterson R. T., In vivo drug discovery in the zebrafish Nature Reviews Drug Discovery 2005 4 1 35 44 (Pubitemid 40109588)
50. Spitsbergen J. M., Kent M. L., The state of the art of the zebrafish model for toxicology and toxicologic pathology researchadvantages and current limitations Toxicologic Pathology 2003 31 62 87 (Pubitemid 36169407)
51. Rubinstein A. L., Zebrafish: from disease modeling to drug discovery Current Opinion in Drug Discovery and Development 2003 6 2 218 223 (Pubitemid 36368376)
52. Dooley K., Zon L. I., Zebrafish: a model system for the study of human disease Current Opinion in Genetics and Development 2000 10 3 252 256 (Pubitemid 30307241)
53. Lieschke G. J., Currie P. D., Animal models of human disease: zebrafish swim into view Nature Reviews Genetics 2007 8 5 353 367 (Pubitemid 46625809)
54. Best J. D., Alderton W. K., Zebrafish: an In vivo model for the study of neurological diseases Neuropsychiatric Disease and Treatment 2008 4 3 567 576 (Pubitemid 352037836)
55. Egan R. J., Bergner C. L., Hart P. C., Cachat J. M., Canavello P. R., Elegante M. F., Elkhayat S. I., Bartels B. K., Tien A. K., Tien D. H., Mohnot S., Beeson E., Glasgow E., Amri H., Zukowska Z., Kalueff A. V., Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish Behavioural Brain Research 2009 205 1 38 44
56. Cachat J., Canavello P., Elegante M., Bartels B., Hart P., Bergner C., Egan R., Duncan A., Tien D., Chung A., Wong K., Goodspeed J., Tan J., Grimes C., Elkhayat S., Suciu C., Rosenberg M., Chung K. M., Kadri F., Roy S., Gaikwad S., Stewart A., Zapolsky I., Gilder T., Mohnot S., Beeson E., Amri H., Zukowska Z., Soignier R. D., Kalueff A. V., Modeling withdrawal syndrome in zebrafish Behavioural Brain Research 2010 208 2 371 376
57. Maximino C., de Brito T. M., Dias C. A., Gouveia A., Morato S., Scototaxis as anxietylike behavior in fish. Nature Protocols 2010 5 2 209 216
58. Stewart A., Kadri F., DiLeo J., The developing utility of zebrafish in modeling neurobehavioral disorders International Journal of Comparative Psychology 2010 23 104 121
59. Wong K., Elegante M., Bartels B., Elkhayat S., Tien D., Roy S., Goodspeed J., Suciu C., Tan J., Grimes C., Chung A., Rosenberg M., Gaikwad S., Denmark A., Jackson A., Kadri F., Chung K. M., Stewart A., Gilder T., Beeson E., Zapolsky I., Wu N., Cachat J., Kalueff A. V., Analyzing habituation responses to novelty in zebrafish (Danio rerio) Behavioural Brain Research 2010 208 2 450 457
60. Kaslin J., Panula P., Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio) Journal of Comparative Neurology 2001 440 4 342 377 (Pubitemid 33041750)
61. Shin J. T., Fishman M. C., From zebrafish to human: modular medical models Annual Review of Genomics and Human Genetics 2002 3 311 340 (Pubitemid 35217440)
62. Gabriel J. P., Mahmood R., Kyriakatos A., Sll I., Hauptmann G., Calabrese R. L., El Manira A., Serotonergic modulation of locomotion in zebrafish: endogenous release and synaptic mechanisms Journal of Neuroscience 2009 29 33 10387 10395
63. Mueller T., Vernier P., Wullimann M. F., The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio Brain Research 2004 1011 2 156 169 (Pubitemid 38638682)
64. Panula P., Sallinen V., Sundvik M., Kolehmainen J., Torkko V., Tiittula A., Moshnyakov M., Podlasz P., Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases Zebrafish 2006 3 2 235 247 (Pubitemid 43979333)
65. Gerlai R., Lee V., Blaser R., Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio) Pharmacology Biochemistry and Behavior 2006 85 4 752 761 (Pubitemid 46151719)
66. Li G., Chen J., Xie P., Jiang Y., Wu L., Zhang X., Protein expression profiling in the zebrafish (Danio rerio) embryos exposed to the microcystin-LR Proteomics 2011 11 10 2003 2018
67. Zhao Y., Xiong Q., Xie P., Analysis of microRNA expression in embryonic developmental toxicity induced by MC-RR PLoS One 2011 6 7
68. Oberholster P. J., Myburgh J. G., Govender D., Bengis R., Botha A. M., Identification of toxigenic Microcystis strains after incidents of wild animal mortalities in the Kruger National Park, South Africa Ecotoxicology and Environmental Safety 2009 72 4 1177 1182
69. Backer L. C., McNeel S. V., Barber T., Kirkpatrick B., Williams C., Irvin M., Zhou Y., Johnson T. B., Nierenberg K., Aubel M., LePrell R., Chapman A., Foss A., Corum S., Hill V. R., Kieszak S. M., Cheng Y. S., Recreational exposure to microcystins during algal blooms in two California lakes Toxicon 2010 55 5 909 921
70. Gerlai R., Lahav M., Guo S., Rosenthal A., Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects Pharmacology Biochemistry and Behavior 2000 67 4 773 782 (Pubitemid 32144928)
71. Levin E. D., Bencan Z., Cerutti D. T., Anxiolytic effects of nicotine in zebrafish Physiology Behavior 2007 90 1 54 58 (Pubitemid 44918005)
72. Gerlai R., Zebra fish: an uncharted behavior genetic model Behavior Genetics 2003 33 5 461 468 (Pubitemid 37243293)
73. Piato A. L., Rosemberg D. B., Capiotti K. M., Acute restraint stress in zebrafish: behavioral parameters and purinergic signaling Neurochemical Research 2011 36 10 1876 1886
74. Barcellos L. J. G., Ritter F., Kreutz L. C., Quevedo R. M., da Silva L. B., Bedin A. C., Finco J., Cericato L., Whole-body cortisol increases after direct and visual contact with a predator in zebrafish Danio rerio Aquaculture 2007 272 14 774 778 (Pubitemid 350064296)
75. Oberemm A., Becker J., Codd G. A., Steinberg C., Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians Environmental Toxicology 1999 14 1 77 88
76. Pietsch C., Wiegand C., Amé M. V., Nicklisch A., Wunderlin D., Pflugmacher S., The effects of a cyanobacterial crude extract on different aquatic organisms: evidence for cyanobacterial toxin modulating factors Environmental Toxicology 2001 16 6 535 542 (Pubitemid 33130333)
77. Zala S. M., Penn D. J., Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges Animal Behaviour 2004 68 4 649 664 (Pubitemid 39348045)
78. Saint-Amant L., Drapeau P., Time course of the development of motor behaviors in the zebrafish embryo Journal of Neurobiology 1998 37 4 622 632 (Pubitemid 28549222)
79. Saint-Amant L., Drapeau P., Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling Neuron 2001 31 6 1035 1046 (Pubitemid 32925288)
80. Borla M. A., Palecek B., Budick S., O'Malley D. M., Prey capture by larval zebrafish: evidence for fine axial motor control Brain, Behavior and Evolution 2002 60 4 207 229 (Pubitemid 35404252)
81. Watkins J., Miklosi A., Andrew R. J., Early asymmetries in the behaviour of zebrafish larvae Behavioural Brain Research 2004 151 1-2 177 183 (Pubitemid 38501440)
82. Loucks E., Carvan M. J., Strain-dependent effects of developmental ethanol exposure in zebrafish Neurotoxicology and Teratology 2004 26 6 745 755 (Pubitemid 39296759)
83. Damodaran S., Dlugos C. A., Wood T. D., Rabin R. A., Effects of chronic ethanol administration on brain protein levels: a proteomic investigation using 2-D DIGE system European Journal of Pharmacology 2006 547 13 75 82 (Pubitemid 44373911)
84. Airhart M. J., Lee D. H., Wilson T. D., Miller B. E., Miller M. N., Skalko R. G., Movement disorders and neurochemical changes in zebrafish larvae after bath exposure to fluoxetine (PROZAC) Neurotoxicology and Teratology 2007 29 6 652 664 (Pubitemid 350101084)
85. Pyron M., Female preferences and male-male interactions in zebrafish (Danio rerio) Canadian Journal of Zoology 2003 81 1 122 125 (Pubitemid 36631773)
86. Engeszer R. E., Ryan M. J., Parichy D. M., Learned social preference in zebrafish Current Biology 2004 14 10 881 884 (Pubitemid 38800909)
87. Bass S. L. S., Gerlai R., Zebrafish (Danio rerio) responds differentially to stimulus fish: the effects of sympatric and allopatric predators and harmless fish Behavioural Brain Research 2008 186 1 107 117 (Pubitemid 350100900)
88. Mann K. D., Turnell E. R., Atema J., Gerlach G., Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues The Biological Bulletin 2003 205 2 224 225
89. Vitebsky A., Reyes R., Sanderson M. J., Michel W. C., Whitlock K. E., Isolation and characterization of the laure olfactory behavioral mutant in the zebrafish, Danio rerio Developmental Dynamics 2005 234 1 229 242 (Pubitemid 41192767)
90. Darland T., Dowling J. E., Behavioral screening for cocaine sensitivity in mutagenized zebrafish Proceedings of the National Academy of Sciences of the United States of America 2001 98 20 11691 11696 (Pubitemid 32928790)
91. Ninkovic J., Bally-Cuif L., The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse Methods 2006 39 3 262 274 (Pubitemid 44189881)
92. Kily L. J., Cowe Y. C., Hussain O., Patel S., McElwaine S., Cotter F. E., Brennan C. H., Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways Journal of Experimental Biology 2008 211 10 1623 1634 (Pubitemid 351960100)
93. Cirelli C., Tononi G., Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system Journal of Neuroscience 2000 20 24 9187 9194 (Pubitemid 32042921)
94. Williams F. E., White D., Messer W. S., A simple spatial alternation task for assessing memory function in zebrafish Behavioural Processes 2002 58 3 125 132 (Pubitemid 34597245)
95. Colwill R. M., Raymond M. P., Ferreira L., Escudero H., Visual discrimination learning in zebrafish (Danio rerio) Behavioural Processes 2005 70 1 19 31 (Pubitemid 40828300)
96. Plaut I., Effects of fin size on swimming performance, swimming behaviour and routine activity of zebrafish Danio rerio Journal of Experimental Biology 2000 203 4 813 820 (Pubitemid 30144449)
97. Blaser R., Gerlai R., Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods Behavior Research Methods 2006 38 3 456 469
98. Spence R., Gerlach G., Lawrence C., Smith C., The behavior and ecology of the zebrafish, Danio rerio Biological Reviews of the Cambridge Philosofical Society 2008 83 1 13 34
99. Ward A. J. W., Duff A. J., Currie S., The effects of the endocrine disrupter 4-nonylphenol on the behaviour of juvenile rainbow trout (Oncorhynchus mykiss) Canadian Journal of Fisheries and Aquatic Sciences 2006 63 2 377 382
100. Saglio P., Trijasse S., Behavioral responses to atrazine and diuron in goldfish Archives of Environmental Contamination and Toxicology 1998 35 3 484 491 (Pubitemid 28409359)
101. Xia J., Niu C., Pei X., Effects of chronic exposure to nonylphenol on locomotor activity and social behavior in zebrafish (Danio rerio) Journal of Environmental Sciences 2010 22 9 1435 1440
102. Barton B. A., Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids Integrative and Comparative Biology 2002 42 3 517 525 (Pubitemid 35419987)
103. Piato A. L., Capiotti K. M., Tamborski A. R., Unpredictable chronic stress model in zebrafish (Danio rerio): behavioral and physiological responses Progress in Neuro-Psychopharmacology Biological Psychiatry 2011 35 2 561 567
104. Bury N. R., Eddy F. B., Codd G. A., The stress responses of brown trout, Salmo truffa L, to the cyanobacterium, Microcystis aeruginosa Environmental Toxicology and Water Quality 1996 11 3 187 193
105. Li D., Xie P., Zhang X., Changes in plasma thyroid hormones and cortisol levels in crucian carp (Carassius auratus) exposed to the extracted microcystins Chemosphere 2008 74 1 13 18