Abstract
Clomazone is considered a potential contaminant of groundwater and is persistent in the environment. To verify the effects of clomazone in Cyprinus carpio and Rhamdia quelen, a method that combines biomarker responses into an index of “integrated biomarker response” (IBR) was used for observed biological alterations in these species. Thiobarbituric acid-reactive substances in liver of carp and silver catfish decreased at both concentrations tested. However, in muscle it increased in carp at 3 mg/L and silver catfish at 6 mg/L. Protein carbonyl increased in liver (3 and 6 mg/L) and muscle (6 mg/L) of carp. In carp, superoxide dismutase (SOD) increased at 3 mg/L and catalase at 6 mg/L. In silver catfish, SOD in liver decreased at 3 mg/L. Glutathione-S-transferase increased at 3 mg/L in muscle of carp. Nonprotein thiol levels decreased at both concentrations in liver of silver catfish and muscle of carp. In silver catfish, acetylcholinesterase (AChE) decreased in brain at 6 mg/L. Nevertheless, AChE in muscle of both species increased at 3 and 6 mg/L. IBR was standardized scores of biomarker responses and was visualized using star plots. The IBR values shown that in carp there was predominantly an induction of parameters, whereas in silver catfish there was inhibition of these responses. In this way, IBR may be a practical tool for the identification of biological alterations in fish exposed to pesticides. In the present study, IBR was efficient for comparisons of fish species using clomazone. This study may serve as a base for evaluation of other pesticides in the rice field, environment, or laboratory experiment.
Similar content being viewed by others
References
Almeida LC, Aguiar LH, Moraes G (2005) Methyl parathion effect in Matrinxã Brycon cephalus muscle and brain acetylcholinesterase activity. Ciência Rural 35:1412–1416
Almroth BC, Sturve J, Berglund A, Forlin L (2005) Oxidative damage in eelpout (Zoarces viviparus) measured as protein carbonyls and TBARS, as biomarkers. Aquat Toxicol 73:171–180
Andres A, Concenço G, Theisen G, Vidotto F, Ferrero A (2013) Selectivity and weed control efficacy of pre and post-emergence applications of clomazone in Southern Brazil. Crop Prot 53:103–108
Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322
Bongers ABJ, Sukkel M, Gort G, Komen J, Richter JJ (1998) Development and use of genetically uniforms strain of common carp in experimental animal research. Lab Anim 32:349–363
Bradford MMA (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–309
Cao J, Diao X, Hu J (2013) Hydrolysis and photolysisc of herbicide clomazone in aqueous solutions and natural water under abiotic conditions. J Integr Agric 12:2074–2082
Cattaneo R, Moraes BS, Loro VL, Pretto A, Menezes C, Sartori GMS et al (2012) Tissue biochemical alterations of Cyprinus carpio exposed to commercial herbicide containing clomazone under rice-field conditions. Arch Environ Contam Toxicol 62:97–106
Crestani M, Menezes C, Glusczak L, Miron DS, Spanevello R, Silveira A et al (2007) Effect of clomazone herbicide on biochemical and histological aspects of silver catfish (Rhamdia quelen) and recovery pattern. Chemosphere 67:2305–2311
Damiens G, Gnassia-Barelli M, Loques F, Romeo M, Salbert V (2007) Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels. Chemosphere 66:574–583
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77
Ellman GL, Courtney KD, Andres V Jr (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
EMBRAPA. 2011. Empresa Brasileira de Pesquisa Agropecuária. Comunicado técnico 167: Dissipação do herbicida clomazone na cultura de arroz irrigado em Rio Brilhante, MS. http://www.infoteapproximatelycnptia.embrapa.br/bitstream/doc/901103/1/COT1672011.pdf. Accessed 21 Oct 2013
Filho MVS, Oliveira MM, Salles JB, Bastos VLFC, Cassano VPF, Bastos JC (2004) Methyl-paraoxon comparative inhibition kinetics from brain of neotropical fishes. Toxicol Lett 153:247–254
Glusczak L, Loro VL, Pretto A, Moraes BS, Raabe A, Duarte MF et al (2011) Acute exposure to glyphosate herbicide affects oxidative parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol 61:624–630
Habig WH, Pabst MJ, Jacoby WB (1974) Glutathione S-transferase, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Instituto Rio Grandense do Arroz (2013) Irga divulga estimativa da safra 2013/2014. http://www.irga.rs.gov.br/conteudo/4253/irga-divulga-estimativa-da-safra-2013/2014/termosbusca=produ%C3%A7%C3%A3o. Accessed 21 Oct 2013
Kim WK, Lee SK, Jung J (2010) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180:395–400
Lazartigues A, Thomas M, Banas D, Brun-Bellet J, Cren-Olivé C, Feidt C (2013) Accumulation and half-lives of 13 pesticides in muscle tissue of freshwater fishes through food exposure. Chemosphere 91:530–535
Mabuchi K, Miya M, Senou H, Suzuki T, Nishida M (2006) Complete mitochondrial DNA sequence of the Lake Biwa wild strain of common carp (Cyprinus carpio L.): further evidence for an ancient origin. Aquaculture 257:68–77
Mela M, Guiloski IC, Doria HB, Randi MAF, Ribeiro MAFO, Pereira L et al (2013) Effects of the herbicide atrazine in neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Saf 93:13–21
Menezes CC, Loro VL, Fonseca MB, Cattaneo R, Pretto A, Miron DS et al (2011) Oxidative parameters of Rhamdia quelen in response to commercial herbicide containing clomazone and recovery pattern. Pestic Biochem Physiol 100:145–150
Miron DS, Crestani M, Schetinger MR, Morsch VM, Baldisserotto B, Tierno MA et al (2005) Effects of the herbicide clomazone, quinclorac and metsulfuron methyl on acetylcholinesterase activity in the silver catfish (Rhamdia quelen) (Heptapteridae). Ecotoxicol Environ Saf 61:398–403
Miron DS, Pretto A, Crestani M, Glusczak L, Schetinger MR, Loro VL et al (2008) Biochemical effects of clomazone herbicide on piava (Leporinus obtusidens). Chemosphere 74:1–5
Misra HP, Fridovich I (1972) The role of superoxide anion in the auto-oxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175
Modesto KA, Martinez CBR (2010) Effects of Roundup Transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere 81:781–787
Moraes BS, Loro VL, Glusczak L, Pretto A, Menezes C, Marchezan E et al (2007) Effects of four rice herbicides on some metabolic and toxicology parameters of teleost fish (Leporinus obtusidens). Chemosphere 68:1597–1601
Moraes BS, Loro VL, Pretto A, Fonseca MB, Menezes C, Marchesan E et al (2009) Toxicological and metabolic parameters of the teleost fish (Leporinus obtusidens) in response to commercial herbicides containing clomazone and propanil. Pestic Biochem Physiol 95:57–62
Murussi CR, Thorstenberg ML, Leitemperger J, Costa M, Clasen B, Santi A et al (2014) Toxic effects of penoxsulam herbicide in two fish species reared in southern Brazil. Bull Environ Contam Toxicol 92:81–84
Nelson DP, Kiesow LA (1972) Enthalpy of decomposition of hydrogen peroxide by catalase at 25 °C (with molar extinction coefficients of H2O2 solution in the UV). Anal Biochem 49:474–478
Oropesa AL, García-Cambero JP, Soler F (2009) Glutathione and malondialdehyde levels in common carp after exposure to simazine. Environ Toxicol Pharmacol 27:30–38
Parvez S, Raisuddin S (2005) Protein carbonyl: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctate (Bloch). Environ Toxicol Pharmacol 20:112–117
Parvez S, Raisuddin S (2006) Effects of paraquat on the freshwater fish Channa punctata (Bloch): nonenzymatic antioxidants as biomarkers of exposure. Arch Environ Contam Toxicol 50:392–397
Pereira L, Fernandes MN, Martinez CBR (2013) Hematological and biochemical alterations in the fish Prochilodus lineatus caused by the herbicide clomazone. Environ Toxicol Pharmacol 36:1–8
Pretto A, Loro VL, Menezes CC, Moraes BS, Reimche GB, Zanella R et al (2011) Commercial formulation containing quinclorac and metsulfuron-methyl herbicides inhibit acetylcholinesterase and induce biochemical alterations in tissues of Leporinus obtusidens. Ecotoxicol Environ Saf 74:336–341
Raftopoulou EK, Dimitriadis VK (2010) Assessment of the health status of mussels Mytilus galloprovincialis along Thermaikos Gulf (Northern Greece): an integrative biomarker approach using ecosystem health indices. Ecotoxicol Environ Saf 73:1580–1587
Salbego J, Pretto A, Gioda CR, Menezes CC, Lazzari R, Neto JR et al (2010) Herbicide formulation with glyphosate affects growth acetylcholinesterase activity, and metabolic and hematological parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol 58:740–745
Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated biomarker response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725
Sauco S, Eguren G, Heinzen H, Defeo O (2010) Effects of herbicides and freshwater discharge on water chemistry, toxicity and benthos in a Uruguayan sandy beach. Mar Environ Res 70:300–307
Serafim A, Company R, Lopes B, Fonseca VF, França S, Vasconcelos RP et al (2012) Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecol Indic 19:215–225
Tomco PL, Holstege DM, Zou W, Tjeederma RS (2010) Microbial degradation of clomazone under simulated California rice field conditions. J Agric Food Chem 58:3674–3680
Üner N, Oruç EO, Sevgiler Y, Sahin N, Durmaz H, Usta D (2006) Effects of diazinon on acetylcholinesterase activity and lipid peroxidation in the brain of Oreochromis niloticus. Environ Toxicol Pharmacol 21:241–245
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
Yan LJ, Traber MG, Packer L (1995) Spectrophotometric method for determination of carbonyls in oxidatively modified apolipoprotein B of human low-density lipoproteins. Anal Biochem 228:349–351
Zanella R, Primel EG, Gonçalves GG, Martins AF (2000) Development and validation of a high-chromatographic method for the determination of clomazone residues in surface water. J Chromatogr A 904:257–262
Zanella R, Primel EG, Machado SLO, Gonçalves FF, Marchezan E (2002) Monitoring of the herbicide clomazone in environmental water samples by solid-phase extraction and high-performance liquid chromatography with ultraviolet detection. Chromatographia 55:573–577
Acknowledgments
We thank the Federal University of Santa Maria for the support and facilities and the financial support and fellowships from the Brazilian agency Coordination for the Improvement of Higher Education Personnel.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Murussi, C.R., Costa, M., Menezes, C. et al. Integrated Assessment of Biomarker Response in Carp (Cyprinus carpio) and Silver Catfish (Rhamdia quelen) Exposed to Clomazone. Arch Environ Contam Toxicol 68, 646–654 (2015). https://doi.org/10.1007/s00244-015-0145-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-015-0145-8