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Oxidative stress biomarkers and heart function in bullfrog tadpoles exposed to Roundup Original®

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Abstract

Oxidative stress biomarkers, in vivo heart rate (f H), and contraction dynamics of ventricle strips of bullfrog (Lithobates catesbeiana) tadpoles were evaluated after 48 h of exposure to a sub-lethal concentration (1 ppm) of the herbicide Roundup Original® (glyphosate 41%). The activities of the antioxidant enzymes superoxide dismutase and catalase were increased in the liver and decreased in muscle, while oxidative damage to lipids increased above control values in both tissues, showing that the generation of reactive oxygen species and oxidative stress are involved in the toxicity induced by Roundup®. Additionally, tadpoles’ hyperactivity was associated with tachycardia in vivo, probably due to a stress-induced adrenergic stimulation. Ventricle strips of Roundup®-exposed tadpoles (R-group) presented a faster relaxation and also a higher cardiac pumping capacity at the in vivo contraction frequency, indicating that bullfrog tadpoles were able to perform cardiac mechanistic adjustments to face Roundup®-exposure. However, the lower maximal in vitro contraction frequency of the R-group could limit its in vivo cardiac performance, when the adrenergic-stimulation is present. The association between the high energetic cost to counteract the harmful effects of this herbicide and the induction of oxidative stress suggest that low and realistic concentrations of Roundup® can have an impact on tadpoles’ performance and success, jeopardizing their survival and/or population establishment.

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References

  • Abdullah MP, Daud J, Hong KS, Yew CH (1995) Improved method for the determination of glyphosate in water. J Chromatogr A 697:363–369

    Article  CAS  Google Scholar 

  • Aebi H (1974) Catalase. In: Bergmayer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 671–684

    Google Scholar 

  • Ahmad I, Pacheco M, Santos MA (2006) Anguilla anguilla L. oxidative stress biomarkers: an in situ study of freshwater wetland ecosystem (Pateira de Fermentelos, Portugal). Chemosphere 65:952–962

    Article  CAS  Google Scholar 

  • Ahmad I, Ahmada I, Hamidb T, Fatimaa M, Chandc HS, Jainb SK, Athara M, Raisuddina S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1519:37–48

    Google Scholar 

  • American Veterinary Medical Association (2001) Report of the AVMA panel on euthanasia. J Am Vet Med Assoc 218:669–696

    Article  Google Scholar 

  • Andersen JB, Jensen FB, Wang T (2001) Effects of temperature and oxygen availability on circulating catecholamines in the toad Bufo marinus. Comp Biochem Physiol A 129:473–486

    Article  CAS  Google Scholar 

  • ASTM—American Society for Testing and Materials (2000) Standard guide for conducting acute toxicity tests on test materials with fishes, macroinvertebrates, and amphibians E 729–96. In: Annual Book of Standards, Vol 11.05, Section 11. Philadelphia, PA, pp 220–240

  • Atli G, Alptekin Ö, Tükel S, Canli M (2006) Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol C 143:218–224

    Article  CAS  Google Scholar 

  • Avci A, Kaçmaz M, Durak İ (2005) Peroxidation in muscle and liver tissues from fish in a contaminated river due to a petroleum refinery industry. Ecotoxicol Environ Saf 6:101–105

    Article  CAS  Google Scholar 

  • Bagnyukovaa TV, Vasylkiva OY, Storeyb KB, Lushchaka VI (2005) Catalase inhibition by amino triazole induces oxidative stress in goldfish brain. Brain Res 1052:180–186

    Article  CAS  Google Scholar 

  • Banudevi S, Krishnamoorthy G, Venkatataman P, Vignesh C, Aruldhas MM, Arunakaran J (2006) Role of α-tocopherol on antioxidant status in liver, lung and kidney of PCB exposed male albino rats. Food Chem Toxicol 44:2040–2046

    Article  CAS  Google Scholar 

  • Bers DM (2001) Excitation-contraction coupling and cardiac contractile force, 2nd edn. Dordrecht, Kluwer Academic Publishers, p 258

    Google Scholar 

  • Boone MD, James SM (2003) Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecol Appl 13:829–841

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brausch JM, Smith PN (2007) Toxicity of three polyethoxylated tallowamine surfactant formulations to laboratory and field collected fairy shrimp, Thamnocephalus platyurus. Arch Environ Contam Toxicol 52(2):217–221

    Article  CAS  Google Scholar 

  • Bridges CM. (2000) Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Arch Environ Contam Toxicol 39:91–96

    Article  CAS  Google Scholar 

  • Bridges CM (1997) Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl. Env Toxicol Chem 16(9):1935–1939

    Article  CAS  Google Scholar 

  • Broomhall SD (2005) Measuring chemical impacts on amphibians: ecotoxicity and behavioural data in governmental regulation. Appl Herpetol 2:259–285

    Article  Google Scholar 

  • Burggren WW, Feder ME, Pinder A (1983) Temperature and the balance between aerial and aquatic respiration in larvae of Rana berlandieri and Rana catesbeiana. Physiol Zool 56:263–273

    Google Scholar 

  • Calore EE, Perez NM, Herman MM (2007) Morphometric studies of cardiac myocytes of rats chronically treated with an organophosphate. Ecotoxicol Environ Saf 66(3):447–450

    Article  CAS  Google Scholar 

  • Carvalho FT, Velini ED, Negrisoli E, Rossi CVS (2005) Eficácia do carfentrazone-ethyl no controle de plantas aquáticas latifoliadas em caixas-d’água. Planta Daninha 23(2):305–310

    Google Scholar 

  • Çavas T, Konen S (2007) Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis 22(4):263–268

    Article  CAS  Google Scholar 

  • Christin MS, Gendron AD, Brousseau P, Menard L, Marcogliese DJ, Cyr D, Ruby S, Fournier M (2003) Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ Toxicol Chem 22:1127–1133

    Article  CAS  Google Scholar 

  • Clements C, Ralph S, Petras M (1997) Genotoxicity of select herbicides in Rana catesbeiana tadpoles using the alkaline single-cell gel DNA electrophoresis (Comet) assay. Environ Mol Mutagen 29(3):277–288

    Article  CAS  Google Scholar 

  • Collins JP, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Divers Distrib 9:89–98

    Article  Google Scholar 

  • Comporti M (1985) Lipid peroxidation and cellular damage in toxic liver injury. Lab Investig 523:599–623

    Google Scholar 

  • Cox C, Surgan M (2006) Unidentified inert ingredients in pesticides: implications for human and environmental health. Environ Health Persp 114(12):1803–1806

    CAS  Google Scholar 

  • Crouch RK, Gandy SC, Kinsey G (1981) The inhibition of islet superoxide dismutase by diabetogenic drugs. Diabetes 30:235–241

    CAS  Google Scholar 

  • Di Giulio RT, Washiburn PC, Wenning RJ, Winston GW, Jewell CS (1989) Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ Toxocol Chem 8:1103–1123

    Article  CAS  Google Scholar 

  • Dorval J, Hontela A (2003) Role of glutathione redox cycle and catalase in defense against oxidative stress induced by endosulfan in adrenocortical cells of rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharmacol 192:191–200

    Article  CAS  Google Scholar 

  • Driedzic WR, Gesser H (1994) Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature. Physiol Rev 74(1): 221–258

    CAS  Google Scholar 

  • Erlij D, Cetrangolo R, Valadez R (1965) Adrenotropic receptors in the frog. J Pharmacol Exp Ther 149:65–70

    CAS  Google Scholar 

  • Farrell AP, Jones DR (1992) The Heart. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology: the cardiovascular system v 12A. Academic Press Inc., New York, pp 1–88

    Google Scholar 

  • Favari L, Lopez E, Martinez-Tabche L, Diaz-Pardo E (2002) Effect of insecticides on plankton and fish of Ignacio Ramirez reservoir (Mexico): a biochemical and biomagnification study. Ecotoxicol Environ Saf 51:177–186

    Article  CAS  Google Scholar 

  • Feder ME (1983) Responses to acute aquatic hypoxia in larvae of the frog Rana beriandieri. J Exp Biol 104:79–95

    Google Scholar 

  • Fulle S, Protasi F, Di Tano G, Pietrangelo T, Beltramin A, Boncompagni S, Vecchiet L, Fano G (2004) The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol 39:17–24

    Article  CAS  Google Scholar 

  • Gehin A, Guyon C, Nicod L (2006) Glyphosate-induced antioxidant imbalance in HaCaT: the protective effect of vitamins C and E. Environ Toxicol Pharmacol 22:27–34

    Article  CAS  Google Scholar 

  • Georgieva NV (2005) Oxidative stress as a factor of disrupted ecological oxidative balance in biological systems – a review. Bulg J Vet Med 8(1):1–11

    Google Scholar 

  • Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup herbicide. Rev Contam Toxicol 167:35–120

    CAS  Google Scholar 

  • González A, Marín O, Tuinhof R, Smeets WJAJ (2004) Ontogeny of catecholamine systems in the central nervous system of anuran amphibians: an immunohistochemical study with antibodies against tyrosine hydroxylase and dopamine. J Comp Neurol 346(1):63–79

    Article  Google Scholar 

  • Gül S, Belge-Kurutas E, Yildiz E, Sahan A, Doran F (2004) Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dan Lake. Turkey Environ Int 30:605–609

    Article  CAS  Google Scholar 

  • Gurushankara HP, Krishnamurthy SV, Vasudev V (2007) Effect of malathion on survival, growth, and food consumption of Indian cricket frog (Limnonectus limnocharis) tadpoles. Arch Environ Contam Toxicol 52:251–256

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1987) Oxygen toxicity, oxygen radicals, transition metals and disease. J Biochem 219:1–14

    Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Claredon Press, Oxford, p 469

    Google Scholar 

  • Hazarika A, Sarkar SN, Hajare S, Kataria M, Malik JK (2003) Influence of malathion pretreatment on the toxicity of anilofos in male rats: a biochemical interaction study. Toxicology 185:1–8

    Article  CAS  Google Scholar 

  • Hedrick MS, Chen AK, Jessop KL (2005) Nitric oxide changes its role as a modulator of respiratory motor activity during development in the bullfrog (Rana catesbeiana). Comp Biochem Physiol A 142:231–240

    Article  CAS  Google Scholar 

  • Herman CA, Sandoval EJ (1983) Catecholamine effects on blood pressure and heart rate in the American bullfrog, Rana catesbeiana. Gen Comp Endocrinol 52:142–148

    Article  CAS  Google Scholar 

  • Hillman SS (1976) Cardiovascular correlates of maximal oxygen consumption rates in anuran amphibians. J Com Physiol 109:199–207

    CAS  Google Scholar 

  • Hillman SS, Withers PC, Hedrick MS, Kimmel PB (1985) The effects of erythrocythemia on blood viscosity, maximal systemic oxygen transport capacity and maximal rates of oxygen consumption in an amphibian. J Com Physiol 155:577–581

    CAS  Google Scholar 

  • Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N (2004) Toxicity of glyphosate-based pesticides to four. North American Frog Species Environ Toxicol Chem 23(8):1928–1938

    CAS  Google Scholar 

  • Hultberg M (2007) Cysteine turnover in human cell liones is influenced by glyphosate. Environ Toxicol Pharmacol 23:19–22

    Article  CAS  Google Scholar 

  • Jia XX, Burggren WW (1997) Developmental changes in chemoreceptive control of gill ventilation in larval bullfrogs (Rana catesbeiana). II. Sites of O2-sensitive chemoreceptors. J Exp Biol 200:2237–2248

    Google Scholar 

  • Jiang ZY, Woollard ACS, Wolff SP (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange: comparison with the TBA assay and iodometric method. Lipids 26:777–860

    Article  Google Scholar 

  • Jiang ZY, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low-density lipoprotein. Anal Biochem 202(2):384–389

    Article  CAS  Google Scholar 

  • Jimenez BD, Stegeman JJ (1990) Detoxication enzymes as indicators of environmental stress on fish. In: Adams SM (ed) Biological indicators of stress in fish, vol 8. American Fisheries Symposium. Bethesda, Maryland, pp 67–79

  • Johansson M, Piha H, Kylin H, Merila J (2006) Toxicity of six pesticides to common frog (Rana temporaria) tadpoles. Environ Toxicol Chem 25(12):3164–3170

    Article  CAS  Google Scholar 

  • Kavitha P, Rao V (2007) Oxidative stress and locomotor behaviour response as biomarkers for assessing recovery status of mosquito Wsh, Gambusia aYnis after lethal eVect of an organophosphate pesticide, monocrotophos. Pest Biochem Physiol 87:182–188

    Article  CAS  Google Scholar 

  • Kehrer JP (1993) Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 34:21–48

    Article  Google Scholar 

  • Kimmel KB (2004) Adrenergic receptors and the regulation of vascular resistance in bullfrog tadpoles (Rana catesbeiana). J Comp Physiol B 162(5):455–462

    Google Scholar 

  • Kirby S, Burnstock G (1969) Pharmacological studies of the cardiovascular system in the anaesthetized sleepy lizard (Tiliqua rugosa) and toad (Bufo marinus). Comp Biochem Physiol 28:321–331

    Article  CAS  Google Scholar 

  • Kloberg AJ, Fritsche R (2002) Catecholamines are present in larval Xenopus laevis: a potential source for cardiac control. J Exp Zool 292(3):293–303

    Article  CAS  Google Scholar 

  • Koyama Ka., Koyama Ky, Goto K (1997) Cardiovascular effects of a herbicide containing glufosinate and a surfactant: in vitro and in vivo analyses in rats. Toxicol Appl Pharmacol 145:409–414

    Article  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantification. Meth Mol Biol 32:9–15

    CAS  Google Scholar 

  • Lambert MRK (1997) Effect of pesticides on amphibians and reptiles in sub-Saharan Africa. Rev Environ Contam Toxicol 150:31–73

    CAS  Google Scholar 

  • Layland J, Li JM, Shah AM (2002) Role of cyclic GMP-dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes. J Physiol 540:457–467

    Article  CAS  Google Scholar 

  • Leonard AWR, Hyne V, Lim RP, Chapman JC (1999) Effect of endosulfan runoff from cotton fields on macroinvertebrates in the Namoi River. Ecotoxicol Environ Saf 42:125–134

    Article  CAS  Google Scholar 

  • Lewatowski B, Pytkowski B (1987) Cellular mechanisms of the relationship between myocardial force and frequency of contractions. Prog Biophys Mol Biol 50:97–120

    Article  Google Scholar 

  • Lillo RS (1979) Autonomic cardiovascular control during submergence and emergence in bullfrogs. Am J Physiol 237:R210–R216

    CAS  Google Scholar 

  • Liu Y, Zhang Y, Liu J, Huang D (2006) The role of reactive oxygen species in the herbicide acetochlor-induced DNA damage on Bufo raddei tadpole liver. Aquatic Toxicol 78:21–26

    Article  CAS  Google Scholar 

  • Matikainen N, Vornanen M (1992) Effect of season and temperature acclimation on the function of crucian carp (Carassius carassius) heart. J Exp Biol 167:203–220

    Google Scholar 

  • Monsanto Company (1991) Roundup herbicide, material safety data sheet. Monsanto Canada Streetsville, ON, Canada

    Google Scholar 

  • Monteiro DA, Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol 143:141–149

    Article  Google Scholar 

  • Oruç EO, Usta D (2007) Evaluation of oxidative stress responses and neurotoxicity potential of diazinon in different tissues of Cyprinus carpio. Environ Toxicol Pharmacol 23:48–55

    Article  CAS  Google Scholar 

  • Otero J, Toni P, Garcia-Morato YV (1983) Superoxo dismutase: método para su determinación. Rev Iberoam Invest Clin 2:121–127

    Google Scholar 

  • Peña-Llopis S, Ferrando MD, Peña JB (2003) Fish tolerance to organophosphate-induced oxidative stress is dependent on the glutathione metabolism and enhanced by N-acetylcysteine. Aquat Toxicol 65:337–360

    Google Scholar 

  • Perkins PJ, Herman J, Boermans HJ, Stephenson GR (2000) Toxicity of glyphosate and triclopyr using the frog embryo teratogenesis assay-Xenopus. Environ Toxicol Chem 19(4):940–945

    Article  CAS  Google Scholar 

  • Pieniazek D, Bukowska B, Duda W (2004) Comparison of the effect of Roundup Ultra 360 SL pesticide and its active compound glyphosate on human erythrocytes. Pest Biochem Physiol 79:58–63

    Article  CAS  Google Scholar 

  • Relyea RA (2003) Predator cues and pesticides: A double dose of danger for amphibians. Ecol Appl 13(6):1515–1521

    Article  Google Scholar 

  • Relyea RA (2004) Growth and survival of five amphibian species exposed to combinations of pesticides. Environ Toxicol Chem 23(7):1737–1742

    Article  CAS  Google Scholar 

  • Relyea RA (2005a) The lethal impact of Roundup on aquatic and terrestrial amphibians. Ecol Appl 15:1118–112

    Article  Google Scholar 

  • Relyea RA (2005b) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15(2):618–627

    Article  Google Scholar 

  • Relyea RA (2006) Letters to the editor: the impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities: response. Ecol Appl 16(5):2027–2034

    Article  Google Scholar 

  • Risso-de-Faverney C, Devaux A, Lafaurie M, Girard JP, Bailly B, Rahmani R (2001) Cadmium induces apoptosis and genotoxicity in rainbow trout hepatocytes through generation of reactive oxygen species. Aquat Toxicol 53:65–76

    Article  CAS  Google Scholar 

  • Rodrigues BN, Almeida FLS (2005) Guia de Herbicidas, 5th edn. Londrina, Grafmark, p 592

    Google Scholar 

  • Saygili EI, Konukoglu D, Papila S, Aksay T (2003) Levels of plasma vitamin E, vitamin C, TBARS and cholesterol in male patients with colorectal tumors. Biochemistry (Moscow) 68(3):325–328

    Article  CAS  Google Scholar 

  • Schwerte T, Printz E, Regina Fritsche R (2002) Vascular control in larval Xenopus laevis: the role of endothelial-derived factors. J Exp Biol 205:225–232

    CAS  Google Scholar 

  • Shiels H, Farrell AP (1997) The effect of temperature and adrenaline on the relative importance of the sarcoplasmic reticulum in contributing Ca2+ to force development in isolated ventricular trabeculae from rainbow trout. J Exp Biol 1(200):1607–1621

    Google Scholar 

  • Sk UH, Bhattacharya S (2006) Prevention of cadmium induced lipid peroxidation, depletion of some antioxidative enzymes and glutathione by series of novel organoselenocyanates Environ. Toxicol Pharmacol 22:298–308

    CAS  Google Scholar 

  • Smith GR (2001) Effects of acute exposure to a commercial formulation of glyphosate on the tadpoles of two species of anurans. Bull Environ Contam Toxicol 67:483–488

    Article  CAS  Google Scholar 

  • Sparling DW, Matson C, Bickham J, Doelling-Brown P (2006) Toxicity of glyphosate as Glypro and LI700 to red-eared slider (Trachemys scripta elegans) embryos and early hatchlings. Environ Toxicol Chem 25(10):2768–2774

    Article  CAS  Google Scholar 

  • Sys SU, Pellegrino D, Mazza R, Gattuso A, Andries LJ, Tota B (1997) Endocardial endothelium in the avascular heart of the frog: Morphology and role of nitric oxide. J Exp Biol 200:3109–3118

    CAS  Google Scholar 

  • Szarek J, Siwicki A, Andrzejewska A, Terech-Majewska E, Banaszkiewicz T (2000) Effects of the herbicide Roundup on the ultrastructural pattern of hepatocytes in carp (Cyprinus carpio). Mar Environ Res 50(1–5):263–266

    Article  CAS  Google Scholar 

  • Terech-Majewska E, Siwicki AK, Szweda W (2004) Modulative influence of lysozyme dimer on defense mechanisms in the carp (Cyprinus carpio) and European sheatfish (Silurus glanis) after suppression induced by herbicide. Roundup Pol J Vet Sci 7(2):123–128

    Google Scholar 

  • Thompson DG, Wojtaszek BF, Staznik B, Chartrand DT, Stephenson GR (2004) Chemical and biomonitoring to assess potential acute effects of Vision herbicide on native amphibian larvae in forest wetlands. Environ Toxicol Chem 23:843–849

    Article  CAS  Google Scholar 

  • Thompson DG, Solomon KR, Wojtaszek BF, Edginton AN, Stephenson GR (2006) Letters to the editor: the impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 16(5):2022–2027

    Article  Google Scholar 

  • Tsui MTK, Chu LM (2003) Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 52(7):1189–1197

    Article  CAS  Google Scholar 

  • Venturino A, Rosenbaum E, De Castro AC, Anguiano OL, Gauna L, De Schroeder TF, D’Angelo AMP (2003) Biomarkers of effect in toads and frogs. Biomarkers 8:167–186

    Article  CAS  Google Scholar 

  • Wassersug RJ, Paul RD, Feder ME (1981) Cardiorespiratory synchrony in anuran larvae (Xenopus laevis, Pachymedusa dacnicolor, Rana berlandieri). Comp Biochem Physiol 70A:329–334

    Article  Google Scholar 

  • Withers PC, Hillman SS (2001) Allometric and ecological relationships of ventricle and liver mass in anuran amphibians. Functional Ecol 15:60–69

    Article  Google Scholar 

  • Wilhelm-Filho D, Giulivi C, Boveris A (1993) Antioxidant defenses in marine fish – I. Teleosts Comp Biochem Physiol C 160:409–413

    Google Scholar 

  • Winston GW (1991) Oxidants and antioxidants in aquatic animals. Comp Biochem Physiol 100C:173–176

    CAS  Google Scholar 

Download references

Acknowledgments

Bullfrog tadpoles were kindly provided by the Estrela breeding colony at Ibaté, São Paulo State, Brazil. The authors are thankful to the field technician Mr. Angelo Carnelosi for caring for the tadpoles in the laboratory. All the experiments were performed complying with the Brazilian laws.

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Costa, M.J., Monteiro, D.A., Oliveira-Neto, A.L. et al. Oxidative stress biomarkers and heart function in bullfrog tadpoles exposed to Roundup Original® . Ecotoxicology 17, 153–163 (2008). https://doi.org/10.1007/s10646-007-0178-5

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