Advertisement

Environmental Science and Pollution Research

, Volume 23, Issue 18, pp 18858–18868 | Cite as

Resilience assessment of a biological early warning system based on the locomotor behavior of zebrafish (Danio rerio)

  • Miguel Fernandes
  • João Amorim
  • Vitor Vasconcelos
  • Luis Oliva Teles
Research Article

Abstract

With the development of new tools such as biological early warning systems, it becomes extremely important to test their reliability and detection capability. This work aimed at testing the sturdiness of a video tracking system by determining whether the detection capability does not deteriorate over time, after successive exposures of the zebrafish to three different toxicants, namely sodium hypochlorite, bisphenol A, and ethanol. Zebrafish were exposed to the three tested compounds separately (one fish, one toxicant) once a day, for 1 h and 30 m over 9 days, to 9 % of the 96 h LC50 of the respective toxicant. The behavior analysis was based on nine movement descriptor parameters of the fish, namely: angular velocity; linear velocity; spatial dispersion; linear acceleration; and angular acceleration. A statistical method was developed using self-organizing map (SOM), correspondence analysis, and linear and orthogonal multiple regression models. The results indicated that the system was able to successfully detect the three toxicants. With ethanol, the detection capability was maintained, but in the case of the sodium hypochlorite and bisphenol A, a deterioration of the detection capability occurred over the 9 days. This effect may be due to the induction of detoxification mechanisms and physiological acclimation, or due to the accumulation of adverse effects caused by the repeated exposure to the toxicants. Future works, especially those focusing on the application of similar early warning systems in real-world scenarios, should regularly exchange the sentinel organisms, to avoid degradation of the detection capability, as verified with two of the three tested compounds.

Keywords

Biological early warning system Video tracking Sodium hypochlorite Bisphenol A Ethanol Zebrafish 

Notes

Acknowledgments

This research was partially funded by UID/Multi/04423/2013 project from Fundação para a Ciência e Tecnologia.

References

  1. Ayele D, Zewotir T, Mwambi H (2014) Multiple correspondence analysis as a tool for analysis of large health surveys in African settings. Afr Health Sci 14:1036–1045CrossRefGoogle Scholar
  2. Bae MJ, Park YS (2014) Biological early warning system based on the responses of aquatic organisms to disturbances: a review. Sci Total Environ 466–467:635–649CrossRefGoogle Scholar
  3. Befyaeva NF, Kashirtseva VN, Medvedeva NV, Ipatova OM, Archakov AI, Khudoklinova YY (2010) Zebrafish as a model system for biomedical studies. Biomeditsinskaya Khimiya 56:120–131CrossRefGoogle Scholar
  4. Blaser R, Gerlai R (2006) Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods. Behav Res Methods 38:456–469CrossRefGoogle Scholar
  5. Box GEP, Hunter WG, Hunter JS (1978) Statistics for experimenters : an introduction to design, data analysis, and model building. John Wiley & Sons, New YorkGoogle Scholar
  6. Brewer SK, Little EE, DeLonay AJ, Beauvais SL, Jones SB, Ellersieck MR (2001) Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncorynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Arch Environ Contam Toxicol 40:70–76CrossRefGoogle Scholar
  7. Cabrera C, Ortega E, Lorenzo ML, Lopez MC (1998) Cadmium contamination of vegetable crops, farmlands, and irrigation waters. Rev Environ Contam Toxicol 154:55–81Google Scholar
  8. Chen T-H, Wang Y-H, Wu Y-H (2011) Developmental exposures to ethanol or dimethylsulfoxide at low concentrations alter locomotor activity in larval zebrafish: Implications for behavioral toxicity bioassays. Aquat Toxicol 102:162–166CrossRefGoogle Scholar
  9. Chon T-S (2011) Self-organizing maps applied to ecological sciences. Ecol Inform 6:50–61CrossRefGoogle Scholar
  10. Chon TS, Chung N, Kwak IS, Kim JS, Koh SC, Lee SK, Leem JB, Cha EY (2005) Movement behaviour of Medaka (Oryzias latipes) in response to sublethal treatments of diazinon and cholinesterase activity in semi-natural conditions. Environ Monit Assess 101:1–21Google Scholar
  11. Cousins IT, Mackay D, Staples CA, Klečka GM (2002) A multimedia assessment of the environmental fate of bisphenol A. Hum Ecol Risk Assess 8:1107–1135CrossRefGoogle Scholar
  12. Decreto-Lei 113/2013 do Ministério da Agricultura, do Mar, do Ambiente e do Ordenamento do Território de 7 de Agosto de 2013 relativa à proteção dos animais utilizados para fins científicos [2013].Google Scholar
  13. Delcourt J, Becco C, Vandewalle N, Poncin P (2009) A video multitracking system for quantification of individual behavior in a large fish shoal: Advantages and limits. Behav Res Methods 41:228–235CrossRefGoogle Scholar
  14. Directive 2010/63/EU of the European Parlament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes [2010] L 276/33.Google Scholar
  15. Dlugos CA, Brown SJ, Rabin RA (2011) Gender differences in ethanol-induced behavioral sensitivity in zebrafish. Alcohol 45:11–18CrossRefGoogle Scholar
  16. Dlugos CA, Rabin RA (2003) Ethanol effects on three strains of zebrafish: Model system for genetic investigations. Pharmacol Biochem Behav 74:471–480CrossRefGoogle Scholar
  17. Emmanuel E, Perrodin Y, Blanchard JM, Vermande P, Keck G (2004) Toxicological effects of disinfections using sodium hypochlorite on aquatic organisms and its contribution to AOX formation in hospital wastewater. Environ Int 30:891–900CrossRefGoogle Scholar
  18. Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol a exposure, effects, and policy: a wildlife perspective. J Environ Manage 104:19–34CrossRefGoogle Scholar
  19. Gerlai R, Fernandes Y, Pereira T (2009) Zebrafish (danio rerio) responds to the animated image of a predator: towards the development of an automated aversive task. Behav Brain Res 201:318–324CrossRefGoogle Scholar
  20. Gerlai R, Lahav M, Guo S, Rosenthal A (2000) Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol Biochem Behav 67:773–782CrossRefGoogle Scholar
  21. Gerlai R, Lee V, Blaser R (2006) Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio). Pharmacol Biochem Behav 85:752–761CrossRefGoogle Scholar
  22. Goulding AT, Shelley LK, Kennedy CJ, Ross PS (2013) Reduction in swimming performance in juvenile rainbow trout (Oncorhynchus mykiss) following sublethal exposure to pyrethroid insecticides. Comp Biochem Physiol C Toxicol Pharmacol 157:280–286CrossRefGoogle Scholar
  23. Hartmann, C. Bisphenol A: Environmental Fate and Behaviour, Human Health Effects Implications for EU-chemical Policy. Vien: University of Vien. 2012. Master’s thesis.Google Scholar
  24. Hellou J (2011) Behavioural ecotoxicology, an “early warning” signal to assess environmental quality. Environ Sci Pollut Res Int 18:1–11CrossRefGoogle Scholar
  25. Houtman CJ (2010) Emerging contaminants in surface waters and their relevance for the production of drinking water in Europe. J Integr Environ Sci 7:271–295CrossRefGoogle Scholar
  26. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252–4263Google Scholar
  27. Lahnsteiner F, Berger B, Kletzl M, Weismann T (2005) Effect of bisphenol A on maturation and quality of semen and eggs in the brown trout, Salmo trutta f. fario. Aquat Toxicol 75:213–224CrossRefGoogle Scholar
  28. Lindholst C, Bjerregaard P, Wynne PM, Marriott P, Pedersen SN (2003) Metabolism of bisphenol A in zebrafish (Danio rerio) and rainbow trout (Oncorhynchus mykiss) in relation to estrogenic response. Comp Biochem Physiol C Toxicol Pharmacol 135:169–177CrossRefGoogle Scholar
  29. Little E, Archeski R, Flerov B, Kozlovskaya V (1990) Behavioral indicators of sublethal toxicity in rainbow trout. Arch Environ Contam Toxicol 19:380–385CrossRefGoogle Scholar
  30. Liu Y, Chon TS, Lee SH (2011) Analysis of behavioral changes of zebrafish (Danio rerio) in response to formaldehyde using Self-organizing map and a hidden Markov model. Ecol Model 222:2191–2201CrossRefGoogle Scholar
  31. López-Galindo, C., Nebot, E., Rubio, D., Vargas-Chacoff, L., Mancera, J.M., Casanueva, J.F., and Solé, M. (2010a). Biomarker responses in Solea senegalensis exposed to sodium hypochlorite used as antifouling. Chemosphere 78, 885-893.Google Scholar
  32. López-Galindo, C., Nebot, E., Rubio, D., Vargas-Chacoff, L., Mancera, J.M., Casanueva, J.F., and Solé, M. (2010b). Sublethal responses of the common mussel (Mytilus galloprovincialis) exposed to sodium hypochlorite and Mexel®432 used as antifoulants. Ecotoxicology and environmental safety 73, 825-834.Google Scholar
  33. Magalhães P, Armando da Cunha R, Albuquerque dos Santos JA, Buss DF, Baptista DF (2007) Behavioral response of zebrafish Danio rerio Hamilton 1822 to sublethal stress by sodium hypochlorite: ecotoxicological assay using an image analysis biomonitoring system. Ecotoxicology 16:417–422CrossRefGoogle Scholar
  34. Mandich A, Bottero S, Cevasco A, Massari A, Pedemonte F, Benfenati E, Maggioni S, Erratico C, Viganò L (2007) In vivo exposure of carp to graded concentrations of bisphenol A. Gen Comp Endocrinol 153:15–24CrossRefGoogle Scholar
  35. Martins J, Teles LO, Vasconcelos V (2007) Assays with Daphnia magna and Danio rerio as alert systems in aquatic toxicology. Environ Int 33:414CrossRefGoogle Scholar
  36. Nimkerdphol K, Nakagawa M (2008) Effect of sodium hypochlorite on zebrafish swimming behavior estimated by fractal dimension analysis. J Biosci Bioeng 105:486–492CrossRefGoogle Scholar
  37. Oliva Teles L, Fernandes M, Amorim J, Vasconcelos V (2015) Video-tracking of zebrafish (danio rerio) as a biological early warning system using two distinct artificial neural networks: probabilistic neural network (PNN) and self-organizing map (SOM). Aquat Toxicol 165:241–248CrossRefGoogle Scholar
  38. Pitanga, F.L. The effect of sodium hypochlorite in different aquatic organisms. Aveiro: University of Aveiro, 2011. Master’s thesis.Google Scholar
  39. Pittman JT, Ichikawa KM (2013) iPhone(R) applications as versatile video tracking tools to analyze behavior in zebrafish (Danio rerio). Pharmacol Biochem Behav 106:137–142CrossRefGoogle Scholar
  40. Qiao J, Han H (2010) An adaptative fuzzy neural network based on self-organizing Map (SOM). in self-organizing maps. InTech, China, pp 1–14Google Scholar
  41. Reyhanian N, Volkova K, Hallgren S, Bollner T, Olsson PE, Olsen H, Hallstrom IP (2011) 17alpha-Ethinyl estradiol affects anxiety and shoaling behavior in adult male zebra fish (Danio rerio). Aquat Toxicol 105:41–48CrossRefGoogle Scholar
  42. Saili KS, Corvi MM, Das SR, Przybyla J, Anderson KA, Tanguay RL, Weber DN, Patel AU (2012) Neurodevelopmental low-dose bisphenol A exposure leads to early life-stage hyperactivity and learning deficits in adult zebrafish. Toxicology 291:83–92CrossRefGoogle Scholar
  43. Snedecor, G.W., Cochran, W.G., and agricole, A.d.c.t. (1984). Méthodes statistiques (Association de Coordination Technique Agricole).Google Scholar
  44. Spink A, Tegelenbosch R, Buma M, Noldus L (2001) The EthoVision video tracking system a tool for behavioral phenotyping of transgenic mice. Physiol Behav 73:731–744CrossRefGoogle Scholar
  45. StatSoft (2012). STATISTICA (data analysis software system) (version 11. www.statsoft.com.).
  46. Tran S, Gerlai R (2013) Time-course of behavioural changes induced by ethanol in zebrafish (Danio rerio). Behav Brain Res 252:204–213CrossRefGoogle Scholar
  47. Tran S, Chatterjee D, Gerlai R (2014) An integrative analysis of ethanol tolerance and withdrawal in zebrafish (Danio rerio). Behav Brain Res 276:161–170CrossRefGoogle Scholar
  48. Vogl C, Spieser OH, Grillitsch B, Scholz W, Wytek R (1999) Qualification of spontaneous undirected locomotor behavior of fish for sublethal toxicity testing. Part I. Variability of measurement parameters under general test conditions. Environ Toxicol Chem 18:2736CrossRefGoogle Scholar
  49. Wang X, Dong Q, Chen Y, Jiang H, Xiao Q, Wang Y, Li W, Bai C, Huang C, Yang D (2013) Bisphenol A affects axonal growth, musculature and motor behavior in developing zebrafish. Aquat Toxicol 142–143:104–113Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Miguel Fernandes
    • 1
  • João Amorim
    • 1
  • Vitor Vasconcelos
    • 1
    • 2
  • Luis Oliva Teles
    • 1
    • 2
  1. 1.Departamento de BiologiaFaculdade de Ciências da Universidade do PortoPortoPortugal
  2. 2.CIIMAR, Centro Interdisciplinar de Investigação Marinha e AmbientalPortoPortugal

Personalised recommendations