Effects of Bisphenol A on the Expression of CYP1A Transcripts in Juvenile False Clown Anemonefish (Amphiprion ocellaris)
DOI:
https://doi.org/10.14456/gag.2020.8Keywords:
biomarker; BPA; clownfish, cyp1a; qRT-PCRAbstract
Bisphenol A (BPA), used in the manufacturing of various plastic products, is widely distributed in the marine environment and significantly impacts aquatic wildlife. In this study, juvenile false clown anemonefish (Amphiprion ocellaris) was used as a model species for low-dose BPA exposure, and to examine the cytochrome P450 1A gene (cyp1a) as a potential biomarker. Fish were exposed to BPA at a range of concentrations for up to 48 hours. Quantification of BPA in the exposed animals revealed that accumulation was significantly higher in the liver than in the muscle. Therefore, liver tissue was selected for further study. In addition to this, the selection of an appropriate reference gene for quantitative real-time reverse transcription-polymerase chain reaction (qRT-PCR) was investigated. Our results showed that ribosomal protein l8 gene (rp18) was the most stable reference gene, compared to 18S ribosomal RNA gene (18S rRNA) and elongation factor 1α gene (EF-1α). This was used as an internal control in the qRT-PCR experiments. Following exposure to BPA, cpy1a expression significantly increased in a dose- and time-dependent manner: after 24 hours exposure to 50 ng/l BPA, it increased 2.82-fold; and after 12 hours exposure to 100 ng/l BPA, it increased 3.44-fold. A low dose of BPA rapidly induces cyp1a expression in this sentinel species. Thus, cyp1a could be used as a potential biomarker for BPA exposure.
References
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Li Z, Guo J-Y, Li X, Zhou H-J, Zhang S-H, Liu X-D, Chen D-Y, Fang Y-C, Feng X-Z (2017) Behavioral effect of low-dose BPA on male zebrafish: tuning of male mating competition and female mating preference during courtship process. Chemosphere 169: 40–52.
Mirzajani H, Cheng C, Wu J, Chen J, Eda S, Aghdam NE (2017) Ghavifekr BH. A highly sensitive and specific capacitive aptasensor for rapid and label-free trace analysis of bisphenol A (BPA) in canned foods. Biosens Bioelectron 89: 1059–1067.
Canesi L, Fabbri F (2015) Environmental effects of BPA: Focus on aquatic species. Dose Response 13: 996¬–1004.
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: 213–224.
Aluru N, Leatherland JF, Vijayan MM (2010) Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout. Public Library of Science One 5: 1–10.
Alexander HC, Dill DC, Smith LW, Guiney PD, Dorn PB, Dorn PB (1988) Bisphenol A: acute aquatic toxicity. Environmental Toxicology Chemistry 7: 19–26.
Kang J-H, Kantayama Y, Kondo F (2006) Biodegradation or metabolism of bisphenol A: from microorganisms to mammals. Toxicology 217: 81–90.
Drastichová J., Svobodová Z., Groenland M., Dobsíková R., Zlábek V., Weissová D., Szotkowská M. (2005) Effect of Exposure to Bisphenol A and 17ß-estradiol on the SexDifferentiation in Zebrafish (Danio rerio). Acta Vet. Brno 74: 287–291.
Chen J, Xiao Y, Gai Z, Li R, Zhu Z, Bai C, Tanguay RL, Xu X, Huang C, Dong Q. (2015) Reproductive toxicity of low level bisphenol A exposures in a two-generation zebrafish assay: evidence of male-specific effects. Aquat Toxicol. 169: 204–214.
Madhu R, Madhu K, Retheesh T (2012) Life history pathways in false clown Amphiprrion ocellaris Cuvier, 1830: A journey from egg to adult under captive condition. J Mar Biol Ass India 5: 77–90.
Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manage 104: 19–34.
Xu EGB, Morton B, Lee JHW, Leung KMY (2015) Environmental fate and ecological risks of nonylphenols and bisphenol A in the Cape D'Aguilar Marine Reserve, Hong Kong. Mar Pollut Bull: 1–10.
Duong CN, Ra JS, Cho J, Kim SD, Choi HK, Park JH, Kim KW, Inam E, Kim SD (2010) Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78: 286–293.
Ocharoen Y, Boonphakdee C, Boonphakdee T, Shinn AP, Moonmangmee S (2018) High levels of the endocrine disruptors bisphenol-A and 17β-estradiol detected in populations of green mussel, Perna viridis, cultured in the Gulf of Thailand. Aquaculture 497: 348–356.
van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13: 57–149.
Lee C-C, Jiang L-Y, Kuo Y-L, Chen C-Y, Hsieh C-Y, Hung C-F, Tirn C-J (2015) Characteristics of nonylphenol and bisphenol A accumulation by fish and implications for ecological and human health. Sci Total Environ 502: 417–425.
Zheng B, Lei K, Lui R, Song S, An L (2014) Integrated biomarkers in wild crucian carp for early warning of water quality in Hun River, North China. J Environ Sci (China) 26: 909–916.
Stephenson F (2016) Calculations for Molecular Biology and Biotechnology. 3rd ed. Elsevier, London.
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) QBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8: 1–14.
Kim HN, Park KS, Lee SK, Gu MB (2008) Gene expression characteristics in the Japanese Medaka (Oryzias latipes) liver after exposure to endrocrine disrupting chemical. Advanced Environmental monitorin: 338–347.
Boonphakdee C, Ocharoen Y, Shinn AP, Suanla S, Thamnawasolos J (2019) 18S rRNA, a potential reference gene in the qRT-PCR measurement of bisphenol A contamination in green mussels (Perna viridis) collected from the Gulf of Thailand. Agr Nat Resour 53: 652–661.
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: 1–12.
Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56:2907-2914.
Kim R-O, Kim B-M, Hwang D-S, Au DWT, Jung J-H, Shim WJ, Leung KMY, Wu RSS, Rhee J-S, Lee J-S (2013) Evaluation of biomarker potential of cytochrome P450 1A (CYP1A) gene in the marine medaka, Oryzias melastigma exposed to water-accommodated fractions (WAFs) of Iranian crude oil. Comp Biochem Physiol C Toxicol Pharmacol 157: 172–182.
Olsvik PA, Skjærven KH, Søfteland L (2017) Metabolic signatures of bisphenol A and genistein in Atlantic salmon liver cells. Chemosphere 189: 730–743.
Fisher MA, Mehne C, Means JC, Ide CF (2006) Induction of CYP1A mRNA in Carp (Cyprinus carpio) from the Kalamazoo River polychlorinated biphenyl-contaminated superfund site and in a laboratory study. Arch Environ Contam Toxicol 50: 14–22.
Salvo LM, Bainy AC, Ventura EC, Marques MR, Silva JR, Klemz C, Silva de Assis HC (2012) Assessment of the sublethal toxicity of organochlorine pesticide endosulfan in juvenile common carp (Cyprinus carpio). J Environ Sci Health A Tox Hazard Subst Environ Eng 47: 1652–1648.
Karaca M, Varışlı L, Korkmaz K, Özaydın O, Perçin F, Orhan H (2014) Organochlorine pesticides and antioxidant enzymes are inversely correlated with liver enzyme gene expression in Cyprinus carpio. Toxicol Lett 230: 198–207.
Gatidou G, Vassalou E, Thomaidis NS (2010) Bioconcentration of selected endocrine disrupting compounds in the Mediterranean mussel, Mytilus galloprovincialis. Mar Pollut Bull 60: 2111–2116.
Zhou Q, Wu W, Huang Y (2017) TiO2 nanotube array micro-solid phase equilibrium extraction for the determination of bisphenol A, 4-n-nonylphenol, and 4-tert-octylphenol at trace levels with high-performance liquid chromatography. Analytical Methods 20: 8396–8402.
Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509–515.
Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Bio 7: 1–9.
Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer 64: 5245–5250.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] Method. Methods 25: 402–408.
Lindholst C, Pedersen KL, Pedersen SN (2000) Estrogenic response of bisphenol A in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 48: 87–94.
Mita L, Bianco M, Viggiano E, Zollo F, Bencivenga U, Sica V, Monaco G, Portaccio M, Diano N, Colonna A, et al. (2011) Bisphenol A content in fish caught in two different sites of the Tyrrhenian Sea (Italy). Chemosphere 82: 405–410.
Belfroid A,van Velzen M, van der Horst B, Vethaak D (2002) Occurrence of bisphenol A in surface water and uptake in fish: evaluation of field measurements. Chemosphere 49: 97–103.
Muldoon BM, Hogan NS (2016) Biomarker responses to estrogen and androgen exposure in the brook stickleback (Culaea inconstans): A new bioindicator species for endocrine disrupting compounds. Comp Biochem Physiol C Toxicol Pharmacol 180: 1–10.
Nolan T, Hands RE, Bustin, SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1: 1559–1582.
Valenzuela-Castillo A, MendoZa-Cano F, Enriquez-Espinosa T, Grijalva-chon JM, Sanchez-Paz A (2017) Selection and validation of candidate reference genes for quantitative real-time RCR studies in the shrimp Penaeus vannamei under viral infection. Mol Cell Probes 33: 42–50.
Tang R, Dodd A, Lai D, McNabb WC, Love DR (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin (Shanghai) 39: 384–390.
Olsvik PA, Lie KK, Jordal A-EO, Nilsen TO, Hordvik I (2005) Evaluation of potential reference gene in real-time RT-PCR studies of Atlantic salmon. BMC Mol Biol: 1–9.
Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E. (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21: 5539–5547.
Panicz R (2016) Validation of reference genes for RT-qPCR analysis of growth hormone receptor and growth hormone expression in the tench (Tinca tinca) fed substituting poultry meal for fish meal. Aquaculture 465: 178–188.
Filby AL, Tyler CR (2007) Appropriate 'housekeeping' genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol Biol: 1–13.
Lee SY, Nam YK (2016) Evaluation of reference genes for RT-qPCR study in abalone Haliotis discus hannai during heavy metal overload stress. Fisheries and Aquatic Science: 1–11.
Sarasquete C, Segner H (2000) Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies. Sci Total Environ 247: 313–332.
Anjos NAD, Schulze T, Brack W, Val AL, Schirmer K, Scholz, S (2011) Identification and evaluation of cyp1a transcript expression in fish as molecular biomarker for petroleum contamination in tropical fresh water ecosystems. Aquatic Toxicology 103: 46–52.
Pinto DP, Chivittz CC, Ferreira RS, Sopezki MS, Zanette J (2015) Beta-naphthoflavone-induced CYP1A expression in the guppy Jenynsia multidentata: Time-dependent response, anesthetic MS-222 effect and fin analysis. Ecotoxicol Environ Saf 113: 38–44.
Environmental Protection Agency (1992) Plastic pellets in the aquatic environment: sources and recommendations. Battelle Ocean Sciences,Washington.
Erler C, Novak J (2010) Bisphenol A exposure: human risk and health policy. J Pediatr Nurs 25: 400–407.
Li Z, Guo J-Y, Li X, Zhou H-J, Zhang S-H, Liu X-D, Chen D-Y, Fang Y-C, Feng X-Z (2017) Behavioral effect of low-dose BPA on male zebrafish: tuning of male mating competition and female mating preference during courtship process. Chemosphere 169: 40–52.
Mirzajani H, Cheng C, Wu J, Chen J, Eda S, Aghdam NE (2017) Ghavifekr BH. A highly sensitive and specific capacitive aptasensor for rapid and label-free trace analysis of bisphenol A (BPA) in canned foods. Biosens Bioelectron 89: 1059–1067.
Canesi L, Fabbri F (2015) Environmental effects of BPA: Focus on aquatic species. Dose Response 13: 996¬–1004.
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: 213–224.
Aluru N, Leatherland JF, Vijayan MM (2010) Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout. Public Library of Science One 5: 1–10.
Alexander HC, Dill DC, Smith LW, Guiney PD, Dorn PB, Dorn PB (1988) Bisphenol A: acute aquatic toxicity. Environmental Toxicology Chemistry 7: 19–26.
Kang J-H, Kantayama Y, Kondo F (2006) Biodegradation or metabolism of bisphenol A: from microorganisms to mammals. Toxicology 217: 81–90.
Drastichová J., Svobodová Z., Groenland M., Dobsíková R., Zlábek V., Weissová D., Szotkowská M. (2005) Effect of Exposure to Bisphenol A and 17ß-estradiol on the SexDifferentiation in Zebrafish (Danio rerio). Acta Vet. Brno 74: 287–291.
Chen J, Xiao Y, Gai Z, Li R, Zhu Z, Bai C, Tanguay RL, Xu X, Huang C, Dong Q. (2015) Reproductive toxicity of low level bisphenol A exposures in a two-generation zebrafish assay: evidence of male-specific effects. Aquat Toxicol. 169: 204–214.
Madhu R, Madhu K, Retheesh T (2012) Life history pathways in false clown Amphiprrion ocellaris Cuvier, 1830: A journey from egg to adult under captive condition. J Mar Biol Ass India 5: 77–90.
Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manage 104: 19–34.
Xu EGB, Morton B, Lee JHW, Leung KMY (2015) Environmental fate and ecological risks of nonylphenols and bisphenol A in the Cape D'Aguilar Marine Reserve, Hong Kong. Mar Pollut Bull: 1–10.
Duong CN, Ra JS, Cho J, Kim SD, Choi HK, Park JH, Kim KW, Inam E, Kim SD (2010) Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78: 286–293.
Ocharoen Y, Boonphakdee C, Boonphakdee T, Shinn AP, Moonmangmee S (2018) High levels of the endocrine disruptors bisphenol-A and 17β-estradiol detected in populations of green mussel, Perna viridis, cultured in the Gulf of Thailand. Aquaculture 497: 348–356.
van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13: 57–149.
Lee C-C, Jiang L-Y, Kuo Y-L, Chen C-Y, Hsieh C-Y, Hung C-F, Tirn C-J (2015) Characteristics of nonylphenol and bisphenol A accumulation by fish and implications for ecological and human health. Sci Total Environ 502: 417–425.
Zheng B, Lei K, Lui R, Song S, An L (2014) Integrated biomarkers in wild crucian carp for early warning of water quality in Hun River, North China. J Environ Sci (China) 26: 909–916.
Stephenson F (2016) Calculations for Molecular Biology and Biotechnology. 3rd ed. Elsevier, London.
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) QBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8: 1–14.
Kim HN, Park KS, Lee SK, Gu MB (2008) Gene expression characteristics in the Japanese Medaka (Oryzias latipes) liver after exposure to endrocrine disrupting chemical. Advanced Environmental monitorin: 338–347.
Boonphakdee C, Ocharoen Y, Shinn AP, Suanla S, Thamnawasolos J (2019) 18S rRNA, a potential reference gene in the qRT-PCR measurement of bisphenol A contamination in green mussels (Perna viridis) collected from the Gulf of Thailand. Agr Nat Resour 53: 652–661.
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: 1–12.
Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56:2907-2914.
Kim R-O, Kim B-M, Hwang D-S, Au DWT, Jung J-H, Shim WJ, Leung KMY, Wu RSS, Rhee J-S, Lee J-S (2013) Evaluation of biomarker potential of cytochrome P450 1A (CYP1A) gene in the marine medaka, Oryzias melastigma exposed to water-accommodated fractions (WAFs) of Iranian crude oil. Comp Biochem Physiol C Toxicol Pharmacol 157: 172–182.
Olsvik PA, Skjærven KH, Søfteland L (2017) Metabolic signatures of bisphenol A and genistein in Atlantic salmon liver cells. Chemosphere 189: 730–743.
Fisher MA, Mehne C, Means JC, Ide CF (2006) Induction of CYP1A mRNA in Carp (Cyprinus carpio) from the Kalamazoo River polychlorinated biphenyl-contaminated superfund site and in a laboratory study. Arch Environ Contam Toxicol 50: 14–22.
Salvo LM, Bainy AC, Ventura EC, Marques MR, Silva JR, Klemz C, Silva de Assis HC (2012) Assessment of the sublethal toxicity of organochlorine pesticide endosulfan in juvenile common carp (Cyprinus carpio). J Environ Sci Health A Tox Hazard Subst Environ Eng 47: 1652–1648.
Karaca M, Varışlı L, Korkmaz K, Özaydın O, Perçin F, Orhan H (2014) Organochlorine pesticides and antioxidant enzymes are inversely correlated with liver enzyme gene expression in Cyprinus carpio. Toxicol Lett 230: 198–207.
Gatidou G, Vassalou E, Thomaidis NS (2010) Bioconcentration of selected endocrine disrupting compounds in the Mediterranean mussel, Mytilus galloprovincialis. Mar Pollut Bull 60: 2111–2116.
Zhou Q, Wu W, Huang Y (2017) TiO2 nanotube array micro-solid phase equilibrium extraction for the determination of bisphenol A, 4-n-nonylphenol, and 4-tert-octylphenol at trace levels with high-performance liquid chromatography. Analytical Methods 20: 8396–8402.
Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509–515.
Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Bio 7: 1–9.
Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer 64: 5245–5250.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] Method. Methods 25: 402–408.
Lindholst C, Pedersen KL, Pedersen SN (2000) Estrogenic response of bisphenol A in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 48: 87–94.
Mita L, Bianco M, Viggiano E, Zollo F, Bencivenga U, Sica V, Monaco G, Portaccio M, Diano N, Colonna A, et al. (2011) Bisphenol A content in fish caught in two different sites of the Tyrrhenian Sea (Italy). Chemosphere 82: 405–410.
Belfroid A,van Velzen M, van der Horst B, Vethaak D (2002) Occurrence of bisphenol A in surface water and uptake in fish: evaluation of field measurements. Chemosphere 49: 97–103.
Muldoon BM, Hogan NS (2016) Biomarker responses to estrogen and androgen exposure in the brook stickleback (Culaea inconstans): A new bioindicator species for endocrine disrupting compounds. Comp Biochem Physiol C Toxicol Pharmacol 180: 1–10.
Nolan T, Hands RE, Bustin, SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1: 1559–1582.
Valenzuela-Castillo A, MendoZa-Cano F, Enriquez-Espinosa T, Grijalva-chon JM, Sanchez-Paz A (2017) Selection and validation of candidate reference genes for quantitative real-time RCR studies in the shrimp Penaeus vannamei under viral infection. Mol Cell Probes 33: 42–50.
Tang R, Dodd A, Lai D, McNabb WC, Love DR (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin (Shanghai) 39: 384–390.
Olsvik PA, Lie KK, Jordal A-EO, Nilsen TO, Hordvik I (2005) Evaluation of potential reference gene in real-time RT-PCR studies of Atlantic salmon. BMC Mol Biol: 1–9.
Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E. (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21: 5539–5547.
Panicz R (2016) Validation of reference genes for RT-qPCR analysis of growth hormone receptor and growth hormone expression in the tench (Tinca tinca) fed substituting poultry meal for fish meal. Aquaculture 465: 178–188.
Filby AL, Tyler CR (2007) Appropriate 'housekeeping' genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol Biol: 1–13.
Lee SY, Nam YK (2016) Evaluation of reference genes for RT-qPCR study in abalone Haliotis discus hannai during heavy metal overload stress. Fisheries and Aquatic Science: 1–11.
Sarasquete C, Segner H (2000) Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies. Sci Total Environ 247: 313–332.
Anjos NAD, Schulze T, Brack W, Val AL, Schirmer K, Scholz, S (2011) Identification and evaluation of cyp1a transcript expression in fish as molecular biomarker for petroleum contamination in tropical fresh water ecosystems. Aquatic Toxicology 103: 46–52.
Pinto DP, Chivittz CC, Ferreira RS, Sopezki MS, Zanette J (2015) Beta-naphthoflavone-induced CYP1A expression in the guppy Jenynsia multidentata: Time-dependent response, anesthetic MS-222 effect and fin analysis. Ecotoxicol Environ Saf 113: 38–44.
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